Get 20M+ Full-Text Papers For Less Than $1.50/day. Subscribe now for You or Your Team.

Learn More →

A unifying model for Neoproterozoic–Palaeozoic exceptional fossil preservation through pyritization and carbonaceous compression

A unifying model for Neoproterozoic–Palaeozoic exceptional fossil preservation through... ARTICLE Received 28 May 2014 | Accepted 4 Nov 2014 | Published 17 Dec 2014 DOI: 10.1038/ncomms6754 A unifying model for Neoproterozoic–Palaeozoic exceptional fossil preservation through pyritization and carbonaceous compression 1 2 3 4 3 5 6 James D. Schiffbauer , Shuhai Xiao , Yaoping Cai , Adam F. Wallace , Hong Hua , Jerry Hunter , Huifang Xu , 7 8 Yongbo Peng & Alan J. Kaufman Soft-tissue fossils capture exquisite biological detail and provide our clearest views onto the rise of animals across the Ediacaran–Cambrian transition. The processes contributing to fossilization of soft tissues, however, have long been a subject of debate. The Ediacaran Gaojiashan biota displays soft-tissue preservational styles ranging from pervasive pyritization to carbonaceous compression, and thus provides an excellent opportunity to dissect the relationships between these taphonomic pathways. Here geochemical analyses of the Gao- jiashan fossil Conotubus hemiannulatus show that pyrite precipitation was fuelled by the degradation of labile tissues through bacterial sulfate reduction (BSR). Pyritization initiated with nucleation on recalcitrant tube walls, proceeded centripetally, decelerated with exhaustion of labile tissues and possibly continued beneath the BSR zone. We propose that pyritization and kerogenization are regulated principally by placement and duration of the decaying organism in different microbial zones of the sediment column, which hinge on post-burial sedimentation rate and/or microbial zone thickness. 1 2 Department of Geological Sciences, University of Missouri, Columbia, Missouri 65211, USA. Department of Geosciences, Virginia Tech, Blacksburg, Virginia 24061, USA. Early Life Institute, State Key Laboratory of Continental Dynamics, and Department of Geology, Northwest University, Xi’an 710069, China. 4 5 Department of Geological Sciences, University of Delaware, Newark, Delaware 19716, USA. Nanoscale Characterization and Fabrication Laboratory, Institute of Critical Technology and Applied Science, Virginia Tech, Blacksburg, Virginia 24061, USA. NASA Astrobiology Institute, Department of Geoscience, University of Wisconsin, Madison, Wisconsin 53706, USA. Department of Geological Sciences, Indiana University, Bloomington, Indiana 47405, USA. Department of Geology and Earth System Science Interdisciplinary Center, University of Maryland, College Park, Maryland 20742, USA. Correspondence and requests for materials should be addressed to J.D.S. (email: schiffbauerj@missouri.edu). NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 1 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 oft-tissue fossils in the geological record are rare relative to provide and locally concentrate necessary chemical constituents. the profusion of shelly hard parts. While shelly organisms Each case of soft-tissue preservation is thus a race between Sproduce mineralized structures in vivo, soft tissues require destructive decay and constructive mineralization processes . authigenic mineralization to enter the fossil record. The factors Superlative fossils occur in a narrow window where neither contributing to soft-tissue mineralization can be partitioned into degradation obliterates nor mineralization overprints important two distinct but complementary categories: those that facilitate biological details, a scenario contingent on both appropriate and those that drive preservation. Facilitating factors are typically settings and rapid stabilization processes. palaeoenvironmental in nature, serving to chemically or Spanning across the Ediacaran–Cambrian transition, when mechanically delay or inhibit aggressive aerobic degradation Konservat–Lagersta¨tten (deposits with exceptional soft-tissue 3 4,5 (noted in ref. 1 as ‘distal environmental and diagenetic preservation ) are most abundant , numerous mineralization 6,7 conditions’). While independently invoked as responsible for pathways fulfil the role of soft-tissue stabilizers . Two of these soft-tissue preservation, facilitating factors are neither mutually pathways—Beecher’s Trilobite-type pyritization (three- exclusive nor sufficient to guarantee fossilization. These dimensional pervasive pyritization) and Burgess Shale-type conditions can only enable soft-tissue preservation, because kerogenization (two-dimensional carbonaceous compression)— delaying degradation is only part of the preservational puzzle. are particularly important. Pervasive pyritization is commonly Driving factors refer to constructive mineralization processes that facilitated by rapid burial, minimal ambient organic material, replicate or stabilize soft tissues (‘proximal causes’ of ref. 1), periodic or persistent anoxia/dysoxia, reactive iron and sulfate ensuring their survivability through geological time and availability, low bioturbation and bacterial sulfate reduction 1,8–14  2– diagenetic alteration. Counterintuitively, many mineralization (BSR)-mediated decay (BSR: CH COO þ SO -2 3 4 – – processes are dependent on microbially mediated degradation to HCO þ HS ). By and large, kerogenization has been attributed to many of the same facilitating conditions, mostly related to rapid burial into anoxic/dysoxic palaeoenvironments . While a d numerous other palaeoenvironmental and diagenetic considerations have been invoked for kerogenization, such as 6,16 17 15,18 interactions with clays or ferrous iron , high alkalinity and oxidant restriction (that is, lack of sulfate for BSR) through early diagenetic sealing (though see also ref. 19), the common 1,6,12,16,20–24 association of kerogenized fossils with pyrite bolsters the interrelationship of these taphonomic processes. Fossils in the late Ediacaran (B551–541 Ma) Gaojiashan Lagersta¨tte illustrate a preservational gradient from pervasive pyritization to compressed kerogenization , including three- dimensional pervasive pyritization, incomplete pyritization and carbonaceous compression with associated pyritization. As such, this Lagersta¨tte offers an opportunity to establish a comprehensive taphonomic model marrying these pathways. To this end, we geochemically investigate the abundant Gaojiashan fossil Conotubus hemiannulatus, which shows preservation in each of these taphonomic styles. Our data form the basis for the proposed unifying model, which invokes sedimentation rate, and Py Ca cement thus time the decaying carcass spends in specific microbial zones, to regulate taphonomic styles along the pyritization–kerogeni- zation gradient. Results General taphonomic observations. Among hundreds of Con- otubus specimens examined in this study, B80% are preserved three-dimensionally through complete or incomplete pyritization (Fig. 1a,b), with the remaining preserved through two-dimen- sional kerogenization (Fig. 1c). Pervasively pyritized Conotubus specimens possess secondary cracks filled with calcite cements, and thin rinds (o20mm) of iron oxide along these cracks (Figs 2g,3c and 4e). Viewed in longitudinal and transverse cross- sections (Figs 2a,3a and 4b), these specimens show a bimodal size distribution of pyrite crystals. Generally, a micrometric size class Figure 1 | Taphonomic representations of Conotubus hemiannulatus. of crystals ranges from B10 to B250mm, and a millimetric size (a) Pervasively pyritized (rusty weathered colour) Conotubus on bedding class of crystals ranges from B800mm to a few mm. Micrometric plane. Scale bar, 5 mm. (b) Longitudinally fractured Conotubus specimen pyrite crystals are mainly found at the outer edge of the fossil showing carbonate cement infill (labelled Ca cement), with pyritized (Figs 2a and 3a) and sometimes along non-continuous central (labelled Py) nested funnel walls visible (arrows). Scale bar, 1 mm. voids (Fig. 3a) or fractures (Figs 2a and 4b), whereas millimetric (c) Specimen of Conotubus preserved as two-dimensional carbonaceous pyrite crystals comprise the bulk of the tube interior (Fig. 2a). In compressions with aluminosilicate coating. Scale bar, 5 mm. (d) Interpretive some cases, millimetric crystals appear to be amalgamations of schematic of Conotubus showing flexible, funnel-in-funnel tube structure micrometric crystals (Fig. 3a). In others, millimetric crystals and morphology. Figures in b,c are reproduced with permission from appear to have subtle textural variations along their outer edges, Elsevier (modified from ref. 28 and ref. 1, respectively). possibly indicative of later overgrowth (Fig. 2b,c). 2 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. Frequency (%) NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE >–19 ‰ Left transverse transect Right transverse transect ade 5 35 –19 to <–21 ‰ Mean = –28.3‰ Mean = –24.0‰ –21 to <–23 ‰ –23 to <–25 ‰ –25 to <–27 ‰ 4 –27 to <–29 ‰ –29 to <–31 ‰ –31 to <–33 ‰ 3 ≤–33 ‰ bc –40 –30 –20 –10 –40 –30 –20 –10 δ S (‰-VCDT) Longitudinal transect Frequency (%) g 0 5 15 25 Mean = –25.5‰ 35 –10 –20 –30 –40 012 3456789 Point position (mm) FeS -Fe-Ca-Si Figure 2 | SEM/EDS and SIMS d S data for Conotubus specimen GJS-Cono001. (a) Backscatter Z-contrast electron micrograph montage of PY longitudinal section, with all SIMS spots (circles) plotted at analysis location. Microdrilling location for IRMS d S assessment indicated by star. Point PY and star colour corresponds to d S bins shown in upper left key. Scale bar, 1 mm. Insets (b,c) at lower left show higher magnification split-frame of PY black rectangle region highlighting subtle textural difference associated with pyrite overgrowth (arrows in each panel); backscatter electron (b) and secondary electron (c) images. Scale bar, 250mm. (d–f) SIMS transects, with dashed lines indicating mean values and histograms showing frequency of points by 1% bins. Note generalized U-shaped profile in d (left transect), with higher values towards fossil edges and lower values centrally located. To show precision of each 10-cycle point sample mean, error bars mark 1 standard error. These errors do not include the analytical uncertainties of the Balmat pyrite standard, which are relatively small. (g) Energy-dispersive X-ray elemental overlay of iron-sulfur (gold), iron but no sulfur (red), calcium (blue) and silicon (green). Map region corresponds to red rectangle in a. Scale bar, 500mm. Transverse transect > –19 ‰ a b Mean = –28.8‰ 4 35 –19 to <–21 ‰ –21 to <–23 ‰ –23 to <–25 ‰ –25 to <–27 ‰ –27 to <–29 ‰ –29 to <–31 ‰ –31 to <–33 ‰ ≤–33 ‰ –40 –30 –20 –10 0 δ S (‰-VCDT) FeS -Fe-Ca-Si Figure 3 | SEM/EDS and SIMS d S data for Conotubus specimen GJS-Cono002. (a) Backscatter Z-contrast electron micrograph montage of PY longitudinal section, with all SIMS spots (circles) plotted at analysis location. Microdrilling location for IRMS d S assessment indicated by star. PY Point and star colour corresponds to d S bins shown in upper left key. Scale bar, 1 mm. (b) SIMS transect, with dashed line indicating mean value, PY and histogram showing frequency of points by 1% bins. To show precision of each 10-cycle point sample mean, error bars mark 1 s.e. These errors do not include the analytical uncertainties of the Balmat pyrite standard, which are relatively small. (c) EDS elemental overlay of iron-sulfur (gold), iron but no sulfur (red), calcium (blue) and silicon (green). Map region corresponds to red rectangle in a. Scale bar, 500mm. NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 3 & 2014 Macmillan Publishers Limited. All rights reserved. δ S (‰-VCDT) Point position (mm) Point position (mm) Frequency (%) ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 –19 to <–21 ‰ ab –21 to <–23 ‰ –23 to <–25 ‰ –25 to <–27 ‰ –27 to <–29 ‰ –29 to <–31 ‰ Frequency (%) cd 0 5 15 25 35 0 5 15 25 35 –10 Diameter Circumference Mean = –21.8‰ Mean = –25.2‰ –20 –30 –40 012345 01 Point position (mm) ef g FeS -Fe Si 2 Ca Figure 4 | SEM/EDS and d S data for Conotubus specimen GJS-Cono003. (a,b) Backscatter Z-contrast electron micrograph montage of transverse PY section, with all SIMS spots (circles) plotted at analysis location. Microdrilling for IRMS d S was made on the reverse side of the specimen at a location PY corresponding to the star. Point and star colour corresponds to d S bins shown in upper right key. Scale bar in a, 2 mm, in b, 500mm. (c,d) SIMS PY circumference and diameter transects, respectively, with dashed lines indicating mean values, and histograms showing frequency of points by 1% bins. 34 34 Circumference d S plot follows clockwise from straight arrow in b. Using dashed red line in b as a reference, note slight separation of d S values: PY PY 34 34 34 higher d S values to the right and lower d S values to the left of the dashed line in b. Diameter d S plot follows top-to-bottom. To show the PY PY PY precision of each 10-cycle point sample mean, error bars mark 1 s.e. These errors do not include the analytical uncertainties of the Balmat pyrite standard, which are relatively small. (e–g) EDS elemental overlay of iron-sulfur (gold), iron but no sulfur (red), calcium (blue) and silicon (green). Map region corresponds to red rectangle in a. Scale bar in g is 500mm, applicable for e and f. Sulfur isotopic data. Pyrite sulfur isotopic values (d S ), Carbon and oxygen isotopic data. Three-dimensionally but PY measured using secondary ion mass spectroscopy (SIMS), range incompletely pyritized Conotubus specimens show an outer rim between –7.6 and –37.9%-VCDT (Supplementary Table 1 and of pyrite, with multiple generations of compositionally distinct Fig. 2a,d–f; Fig. 3a,b; Fig. 4b–d). Although not a hard-and-fast carbonate cements surrounding a central void in the tube interior rule, pyrite with d S values Z–19% tend to be associated with (Fig. 5). In the only chemically analysed cross-section with this PY fractures and/or textural variations in the pyritized fossil, which preservational style but representative of other similarly preserved may correspond to later overgrowth (for instance, see adjacent specimens, the outer first generation cements consist of large red points in Fig. 2a longitudinal transect positioned just below centripetally terminating calcite crystals, indicating inward car- arrows indicating textural variation in Fig. 2b,c). Disregarding bonate growth from the pyrite rim. The inner second generation obvious fracture-associated S-enriched points, the transverse cements are zoned rhombohedral crystals, with alternating d S transects exhibit a generalized U-shaped profile, with ultraviolet-luminescent zones of ferroan dolomite and dull zones PY localization of greater values along the tube-wall edges and lower of dolomite þ calcite. Carbon and oxygen isotopic compositions values towards the center of the fossil (Fig. 2d,e). This pattern is of microlaminae in the host rock and for the two generations of not discernable in all specimens (Figs 3b and 4c,d). Microdrilled fossil carbonate cements were determined (Supplementary pyrite assessed via isotope ratio mass spectroscopy (IRMS) Table 2 and Fig. 6). The mean d Cvalue of the darker coloured yield d S values broadly similar to mean SIMS values microlaminae (6.1 0.9% VPDB) is greater than that of the PY (Supplementary Table 1). Carbonate-associated sulfate sulfur lighter coloured microlaminae (4.4 1.0%) with slight overlap in 34 18 isotopic composition (d S ) of host rock was assessed at ranges, whereas their mean d O values are broadly similar CAS þ 33.6%-VCDT (Supplementary Table 1), comparable to con- (darker microlaminae ¼ –5.4 1.2%; lighter microlaminae ¼ 25 34 temporaneous units in Oman . Thus, D S is appreciably –5.9 0.3%) with mostly overlapping ranges. While similar in CAS-PY high (ranging from þ 41.2 to 71.5%). carbon isotope composition, the cements in the Conotubus 4 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. δ S (‰-VCDT) NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE ab Host rock Laminae CV IC Py rim OC e f Ca-Mg Fe-Si Calcite Dolomite Light laminae Dark laminae Outer cement Inner cement 10 15 20 25 30 Diffraction angle, 2 (degrees) Figure 5 | Ultraviolet photoluminescence and in situ XRD data for Conotubus specimen 1GH2-70A. (a) Overview photomicrograph of transverse slab of Conotubus and surrounding matrix of laminated rock. Note pyrite or iron oxide rim (gold colour), outer carbonate cement (dark colour), inner carbonate cement (light colour) and central void. Scale bar, 10 mm. (b) Backscattered Z-contrast electron micrograph montage of region defined by white rectangle in a. Fine pyrite or iron oxide rim (Py rim) seen as bright discontinuous specks, surrounding carbonate cements (IC: inner cement; OC: outer cement) and central void (CV). Scale bar, 1 mm. (c) Ultraviolet photoluminescence microscopy of black rectangle region in a, showing zoned carbonate crystals in inner cement. Scale bar, 1 mm. Inset (d) shows higher magnification view of white rectangle in c for better detail of crystal zoning. Scale bar, 500mm. (e,f) EDS elemental maps of white rectangle region in b, with calcium (orange) and magnesium (green) overlay shown in e and iron (red) and silicon (blue) overlay shown in f. Scale bar in f is 1 mm, applicable for e.(g) In situ XRD patterns of host rock light- and dark-coloured laminae, outer carbonate cement within fossil and inner carbonate cement within fossil. Characteristic peak positions of calcite and dolomite are shown in orange and green vertical dashed lines, respectively. The strongest diffraction peaks from calcite and dolomite are labelled with C and D , respectively. tube and the host rock have distinct d O values. Between Discussion fossil-interior cement generations, the outer calcite cements have Previous analyses of pyritized Palaeozoic Lagersta¨tten suggest 13 18 13 slightly greater mean d C and d O values (d C ¼ 6.1 0.1%, rapid burial into anoxic sediments, which in turn reduces d O ¼ –8.2 0.2%) than the inner dolomite þ calcite cements bioturbation, impedes organic deterioration and emplaces the 13 18 ± ± (d C ¼ 5.2 0.4%, d O ¼ –9.0 0.2%). decaying carcasses within the sulfidic BSR zone below the oxic-anoxic boundary in the sediment profile. Further, pyritization-conducive sediments typically have low organic Compaction. Three-dimensional preservation of Conotubus carbon content and abundant reactive iron, serving to focus 8,9,13,14,27 BSR and pyrite precipitation on decaying carcasses . allows an estimate of the compaction ratio of the host sediments. Viewed perpendicular to bedding plane, the calcisiltite/calcilutite While the Gaojiashan biota is similar to these younger deposits in that pyritized fossils are found in sediments deposited by microlaminae warp around nearly circular Conotubus tubes (Figs 4a,b,5 and 6). Measurements of microlaminae surrounding rapid burial events , there are some key differences. First, the full pyritization–kerogenization preservational gradient from Conotubus tubes in comparison with their thickness extending beyond the fossil yields an estimated sediment compaction ratio three-dimensional pervasive pyritization to two-dimensional of B1.85:1. Conotubus tubes show negligible compaction, with a kerogenized compressions, with intermediate or admixed major:minor axis ratio of B1.15:1, although an oblate cross- preservational modes, appears to be unique to the Gaojiashan section may be biological . Lagersta¨tte. Second, the tubular fossils of the Gaojiashan biota NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 5 & 2014 Macmillan Publishers Limited. All rights reserved. Relative intensity 104 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 a b Light-coloured lamina below fossil (a) c Light-coloured lamina above fossil (a) Dark-coloured lamina (a) Light-dark laminae (b) Outer cement within conotubus (a) Inner cement within conotubus (a) –9.5 –8.5 –7.5 –6.5 –5.5 –4.5 –3.5 –2.5 δ O (‰-VPDB) 13 18 Figure 6 | Host rock and fossil carbonate IRMS d C and d O data. (a) Microdrill map of slab 1GH2-70A with Conotubus specimen. Scale bar, 13 18 10 mm. (b) Microdrill map of slab (two continuous pieces) without Conotubus fossils. Scale bar, 50 mm. (c) Cross-plot of all d C and d O analyses. Convex hulls and nested convex hulls (shaded) show groupings of data by location of microsampling. Yellow points show light-coloured laminae (single circle below fossil and double circle above fossil in a; dashed circle from slab in b). Blue points show dark-coloured laminae (single circle contiguous to fossil in a; dashed circle from slab in b). Red and green diamonds show outer and inner cements in a, respectively. Keys also applicable for microdrill location maps. 10,28 notably do not retain their most labile soft parts , showing no porewaters with respect to iron sulfide at some distance from the evidence of the soft-bodied organisms that lived within these organic nucleus. The spatial trends in both pyrite crystal tubes. While some sites of pervasive pyritization show glimpses of morphology and d S values of Conotubus fossils are PY highly labile soft-tissue preservation, such as pygnogonid and consistent with centripetal pyrite growth controlled by the 29,30 31 crustacean musculature from the Hu¨nsruck Slate , pervasive diffusion–precipitation dynamics of mineralization . Similar to pyritization of Conotubus only captures the three-dimensional the formation of pyrite rims around chert nodules and 8,31 exterior morphologies of the tubes. The original histology of carbonate concretions , sulfate reducing bacteria (SRB) Conotubus tubes is unknown. However, they have been metabolized a centrally located organic nucleus, in this case the interpreted as supportive, refractory tissues, either non- labile tissues of the Conotubus organism, generating an outward biomineralized or weakly biomineralized . diffusion of sulfide. The sulfide meets with an inward-diffusing Building upon the Raiswell et al. diffusion–precipitation reactive iron sourced from ambient porewater, forming a reaction model for pyritization, we can begin to elucidate the progression front where pyrite-precursor iron monosulfide precipitation of pervasive fossil pyritization and provide insights into early occurs. As this process proceeds, the organic nucleus is diagenetic conditions responsible for the taphonomic styles progressively exhausted, resulting in an inward shift in the observed in the Gaojiashan Lagersta¨tte. According to this reaction front (Supplementary Fig. 1). model , the locus of mineralization is controlled by the One complicating issue, however, is that the recalcitrant tube intersection of two diffusion fields. The first arises as a walls of Conotubus would form a barrier to impede but not consequence of BSR, driving sulfide outward into the sediment entirely halt diffusion, resulting in accumulation of sulfide and porewaters. The second originates from sediment sources, reactive iron on either side of the tube walls. As such, we must carrying reactive iron toward the decaying organic nucleus. The consider another important factor controlling the locus of intersection of these two diffusion fronts results in supersaturated pyritization: heterogeneous nucleation facilitated by an organic 6 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. δ C (‰-VPDB) Sedimentation rate NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE Pervasive pyritization Incomplete pyritization Partial kerogenization/pyritization Diffuse pyrite kerogenization a b c d Sediment–water interface Aerobic NO NO 2+ 2+ Mn Mn Fe/Mn/DN 2– SO SO 2+ 2+ Fe Fe Termination of HS HS Limited pyritization BSR pyritization Kerog. F Fe-S e-S Kerogenization BSR BSR pyritization Carbonate infill comple complex xes es Pyrite overgrowth C CH H Methanogenesis Time Rapid event burial 0 1 2 3 4 10 10 10 10 10 Background sedimentation Conc. (μM) Figure 7 | Pyritization–kerogenization taphonomic gradient. Fossil examples (a–d, upper panels) and proposed taphonomic model (lower panels) with sedimentary microbial zonation. Diagonal lines track the position of the decaying organisms in the sediment column, and the slope of each line represents sedimentation rate. Grey upper diagonal line corresponds to rapid event burial, and black lower diagonal line corresponds to post-burial sedimentation. Brackets indicate the length of time the decaying organism resides in the BSR zone (gold colour), and experiences BSR-mediated pyrite growth, although pyrite overgrowth may continue into underlying methanogenesis zone (blue colour). From left to right, each diagram indicates a shortened residence time in the BSR zone as compared with the previous panel, which could result from either, or both, changes in post-burial sedimentation rate and BSR zone thickness. (a) Pervasively pyritized Conotubus in transverse cross section. Scale bar, 2.5 mm. Diagram shows initial rapid event deposition, followed by slow post-burial sedimentation. (b) Polished transverse cross-section of pyritized Conotubus showing carbonate in the center and thin outer lamina (arrow) representing nested tube wall. Scale bar, 1 mm. Corresponding diagram shows increase in post-burial sedimentation rate and reduction in BSR zone thickness, leading to comparatively earlier termination of pyritization. (c) Specimen of Conotubus with admixed taphonomic mode of pyritization (black arrows) and carbonaceous compression (white arrows). Scale bar, 5 mm. Diagram shows further increase in post-burial sedimentation rate and reduction in BSR zone thickness, yielding partial pyritization and onset of kerogenization once carcass exits BSR zone. (d) Specimen of Conotubus preserved via complete kerogenization with diffuse pyrite. Scale bar, 5 mm. Diagram shows highest post-burial sedimentation rate and thinnest BSR zone, with limited pyritization, and earliest onset of kerogenization. Relative abundances of chemical species at right follows that of refs 47,48 after ref 67. Fe–S complexes – 2 þ curve shows possible continued pyrite overgrowth from downward diffusion of HS /Fe . Figures in a–d are reproduced with permission from Elsevier (modified from ref. 1 and ref. 28). substrate. The individually conserved nested Conotubus tube matrices , significant variations in the surface nucleation rate walls (Figs 1b and 7b) may have promoted pyritization by may occur between biopolymers with similar functionalities, with providing a naturally favourable substrate for the initiation of the specific order of substrate preference depending chiefly on iron sulfide nucleation—an unaccounted-for factor in the supersaturation. traditional model . During the earliest stages of microbially induced degradation, The ability of an organic substrate, such as the tube walls, to when nucleation sites on the tube surface are most abundant, promote mineralization can be readily justified within the pyritization is dominated by precipitation of abundant micro- constructs of classical nucleation theory. For a cube-shaped metric crystals as are observed at the outer edges of the nucleus, the relationship between the free energy barrier opposing Conotubus specimens. The size and location of the crystallites the formation of a stable nucleus in solution (homogeneous case) indicates that the organic tube-wall surface likely plays a role in het and on a foreign substrate is: DG ¼ DG ð Þ, where a directing the onset of nucleation, and that the pyrite super- hom het hom 2a hom and a are the interfacial energies of the homogeneous and saturation state, s, was relatively high as compared with the later het heterogeneous nuclei. Although a depends on the balance stages of mineralization when pyritization proceeds through het between the liquid-nucleus, liquid-substrate and substrate- coarsening of existing crystals rather than formation of new nucleus interfacial tensions, a simple analysis shows that if crystals. This interpretation is supported by the nucleation rate DG =k T  B=s a Ea , the free energy barrier opposing nucleation at a equation, J ¼ Ae ¼ Ae , where A is a pre- hom het n surface is reduced to half of the homogeneous barrier. As exponential constant (whose units represent the number of nucleation rate shows an exponential dependence on DG*, this molecules attaching to a critically-sized nucleus per unit time and translates into a substantial increase in the rate of surface surface area), B is a constant that describes the shape of the nucleation. Indeed, nucleation rates depend strongly on the nucleus, T is temperature, k is the Boltzmann constant, DG* is chemical nature and physical structure of the organic interface. free energy matching the thermodynamic barrier opposing ion activity product For instance, NH terminated surfaces can be completely passive nucleation and s is supersaturation ðln Þ. This solubility product to the formation of amorphous SiO ; however, under identical equation shows that an increase in supersaturation state generally þ – conditions, NH /COO surfaces promote SiO deposition to the results in a higher number of nuclei per unit area of substrate or 3 2 extent that the organic may be coated by a nearly-coherent volume of solution in the case of homogeneous nucleation. As nanoscale layer of amorphous material within a few hours . compared with any soft body tissues of the Conotubus organism, Moreover, as evidenced by calcite nucleation on polysaccharide the tube walls must have provided the most chemically favourable NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 7 & 2014 Macmillan Publishers Limited. All rights reserved. Microbial zonation with sediment depth ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 32,39 13 nucleation sites for initiation of pyrite growth. Pyrite crystals in precipitation . While similar relatively heavy d C values of these regions are isotopically heavier (d S typically 4–25%; host rock and fossil cement render BSR- or BFeR-sourced PY bicarbonate as insignificant contributors, dissolved sulfide is Fig. 2a,d,e) than those in the tube interior, indicating a progressive decline in BSR rate throughout the pyritization observed to enhance crystallization of calcite and dolomite , process and corresponding relaxation in diffusion-limited sulfate possibly contributing to early calcite cementation. In addition, availability. The inferred sulfate limitation in initial pyritization SRB exopolysaccharides commonly incorporate metal cations may seem contradictory to the high D S values (such as Mg and Fe), which could facilitate precipitation of high- CAS-PY (Supplementary Note 1). However, oxidative recycling of sulfide Mg calcite and ankerite . The B2% difference between 14 18 and oxidation of detrital pyrite entrained in microturbidites carbonate cement d O values within the Conotubus specimen 34 13 likely supplied S-depleted sulfate for pyritization, thereby and host carbonates, but broadly similar d C values (Fig. 6c), contributing to the high D S values. As BSR continues suggest that the cements may have been slightly influenced by CAS-PY over time, labile tissues are diminished and BSR necessarily slows diagenetic fluids without significant alteration of carbon isotopic 18 13 because of decreasing availability of metabolizable organic carbon composition. Slightly lower d O and d C values in the inner rather than sulfate exhaustion or deep burial, which would versus outer cements indicates a stronger influence of diagenetic instead yield a shift towards higher d S values. As a result of fluids on the inner cementation, consistent with petrographic PY slowed BSR, sulfide production rate would drop, supersaturation evidence showing a later origin than the outer cements. The levels with respect to iron sulfide would decrease and nucleation relatively small isotopic difference between the cements and would be disfavoured. Thus, iron sulfide precipitation is focused sedimentary matrix suggests that carbonate cementation may on overgrowing existing crystals, leading to the formation of have occurred shortly after the cessation of pyritization, playing a millimetric crystals. During this shift, d S values would constructive preservational role by enhancing the rigidity of PY decrease as the BSR system switches from sulfate limitation to partially pyritized tubes before sediment compaction. organic limitation. The expected result is a U-shaped d S While we have established that both pervasive and incomplete PY profile as observed in some specimens (Fig. 2d,e), although this pyritization must have predated sediment compaction based on profile can be obscured by pyrite overgrowth (see Discussion warping host rock microlaminae encasing the Conotubus fossils, below). we can further constrain the duration of the pyritization process. From the understanding of how the pyritization process To do so, we must consider requisite levels of sulfate, reactive iron proceeds and expectations for resultant sulfur isotopic trends and metabolizable organic material. On the basis of the size of (Supplementary Note 1), we can then shift our focus to resolving Conotubus specimens, with a maximum diameter of 12 mm and the geochemical constraints for pervasive pyritization. With the length of 3–80 mm (ref. 28), the amount of sulfate required for 7 þ Vr first dissociation constant of H S at 1.05  10 (K ¼ [H ] complete pyritization will follow M ¼ 2 , where V is the 2 1 0 sulfate pyrite [HS ]/[H S]) and seawater pH typically constrained to B7.5–8.5, volume of the Conotubus tube, r is the density of pyrite (E5 g per HS is the dominant dissolved sulfide species. Thus, we can write 3  1 cm ) and M is the molar mass of pyrite (E 120 g mol ). 2 þ 0 – þ pyrite the precipitation of pyrite as Fe þ S þ HS -FeS þ H , Using V ¼ p*r *l for the volume of a cylinder, with Conotubus such that the equilibrium solubility product for pyrite is given as radius (r) and length (l) simplified as 5 and 40 mm, the total 2 þ   pH  16.35 K ¼ [Fe ][HS ]/10 ¼ 10 (ref. 36). With activity sp sulfate required is 0.26 moles. The amount of reactive iron needed – 2 þ coefficients for HS and Fe in seawater at 0.67 and 0.26 is 0.13 moles. The amount of organic carbon needed varies by the (ref. 37), we can then calculate the apparent solubility product for electron donor compound used (largely fermentative end pH K ð10 Þ sp 2 0  24 pyrite as K ¼ ¼ 8:110 ðM Þ at the low end of HS products; Supplementary Table 3). For simplicity, we use BSR sp g g 2 þ Fe normal seawater pH. As such, given the Raiswell et al. model of acetate, which, in accordance with the above constraints, requires 0.52 moles of organic C. If we then assume that the assumption of the estimated ratio of reservoir concentrations (C ) 0 0 2 þ – of sulfur to iron, C :C o0.1 (that is, [Fe ]Z10  [HS ]), for interior volume of Conotubus tube is completely full of soft tissue S Fe (an overestimate), with a nested tube-wall thickness of 1 mm localized pyrite formation at the site of decay , reactive iron must be greater than approximately 9  10 M to drive pyrite (Fig. 1b), the volume of soft tissue that contains metabolizable organic material using the same dimensions as above is B2cm . precipitation, well below modern observations of anoxic Assuming that the soft tissue was pure amorphous carbon sediments ato10 M (refs 8,31). Because the majority of the ¨ (density ¼B1.8 g cm ), 0.52 moles would occupy a volume of fossils in the Gaojiashan Lagerstatte exhibit three-dimensional B3.5 cm , a substantially larger volume than is available within pervasive pyritization , we can surmise an excess of available the Conotubus tube. As such, given realistic carbon contents in sediment/porewater reactive iron. Assuming a decay constant animal tissues, we can deduce that there is a deficit of endogenous of 0.1–1.0 per year (reported for organic decay in marine sediments ) and an organic nucleus radius of 0.1–1.0 cm carbon to account for the volume of pyrite precipitated—which is clearly problematic, but disregarded for now and revisited in our (appropriate for Conotubus with a maximum diameter of 1.2 cm (ref. 28)), porewater dissolved sulfide concentrations of model description below. On the basis of these calculations and high-end rates of sulfate reduction in Ediacaran sediments o10 M are required for soft tissue pyritization (Fig. 3 in ref. 31). As localized pyritization of highly labile tissues occurs when (6.935 mmol cm per year according to ref. 42, with pervasive 0 0 2 þ anoxic conditions and higher metabolizability of organics before C :C o0.1 (ref. 31), Fe content in porewater may have been S Fe 32,42–44 3 2 þ up to 10 M. We can thus reasonably constrain porewater Fe the evolution of vascular plants ), we can calculate an 12 – approximate timeframe for generating sufficient HS to content in Gaojiashan sediments between 9  10 M and 10 M, justified by the lack of labile soft-tissue pyritization in pervasively pyritize a Conotubus tube with a 3.14 cm total volume. If the 0.26 moles of SO is derived entirely this Lagersta¨tte. endogenously within a Conotubus tube, a total of 82.8 mmol In incompletely pyritized but three-dimensional Conotubus – 3 HS per cm is required for pyritizing the full volume of the tube. tubes, alkalinity generated during BSR (Supplementary Table 3) At a rate of 6.935 mmol cm per year, a total of B12 years and bacterial Fe(III) reduction (BFeR: CH COO þ 2 þ – 8 Fe(OH) -2 HCO þ8Fe þ 15 OH þ5H O) could would be required to generate enough HS for pyritization. Even 3 3 2 at modern rates of sulfate reduction, such as measured rates of contribute to carbonate infill assuming appropriately basic microenvironmental pH levels to facilitate calcite 0.1 mmol cm per year (ref. 45), this yields 828 years to generate 8 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE – – 34 enough HS for pyritization of moderately sized Conotubus tubes. profile because residual porewater HS tends to have greater d S The decaying organism is a BSR hotspot, which should pull in values. In combination, the observed subtle textural variations 2– 2 þ 34 both SO and Fe from the surrounding microenvironment (Fig. 2b,c) and higher d S values along millimetric crystal 4 PY (as opposed to assumed steady-state equilibrium ), thus these edges may support this alternative scenario. Regardless, the keys cited bulk-sediment rates may overestimate the pyritization time. for complete pyritization are rapid burial and initial pyritization It is important to note, however, that these estimates assume that to maintain structural integrity, followed by prolonged pyrite HS is: (1) a rate-limiting factor for pyrite precipitation and (2) overgrowth within and perhaps below a relatively thick BSR zone entirely derived from BSR in and around the decaying Conotubus to completely fill Conotubus tubes with pyrite. organism in the BSR zone. As discussed below, these assumptions Incomplete but three-dimensional pyritization (Fig. 7b) may not be valid. requires the same facilitating taphonomic conditions as complete From these and previously reported observations , the data pyritization, including rapid placement in the BSR zone and presented herein allow for a pragmatic approach to consider the initiation of pyritization to maintain three-dimensionality, but timing, processes, and interrelationship of pyritization and instead experiences closure of the pyritization process before kerogenization. First, the pyritization process is likely initiated complete infilling of the Conotubus tube with pyrite. As such, in the BSR zone in the sediment column. The sediment column temporal limitation of one or more of the required chemical typically consists of an aerobic respiration zone just beneath the components, such as diffusive extinction of sulfate, may limit the water–sediment interface, followed by an anaerobic zone with extent of the BSR zone. With or without BSR zone restriction, nitrate, manganese and iron reduction, then the BSR zone, and the decaying Conotubus organism is likely pushed down into the finally the methanogenesis zone at depth (Fig. 7). For fossil methanogenesis zone due to high post-burial sedimentation rate, pyritization to occur in the BSR zone, factors directly responsible such that pyritization in the BSR zone is prematurely terminated. for BSR-mediated pyrite mineralization—the availability of Alternatively, these incompletely pyritized tubes may persist sulfate, reactive iron, metabolizable organic material and within the BSR zone, but with cessation of pyritization due to positioning of the carcass within the BSR zone—must overlap exhaustion of metabolizable organic material and a shortage of with commonly invoked facilitating conditions such as rapid exogenous carbon input. The interior space originally occupied by sedimentation and burial, low bioturbation and sediment anoxia. the Conotubus animal then becomes a central void, which is These factors are intimately related. For example, sedimentation subsequently infilled with carbonate cements. The timing of rate influences the availability of reactive iron, sulfate and organic carbonate cementation may depend on the electron donor used in carbon in the sediments, thus controlling the thickness of the BSR BSR (Supplementary Table 3). Two scenarios are plausible: zone and ultimately how much time the decaying carcass spends (1) the BSR respiration pathway does not produce acidity and here. Because sedimentation rate plays such an important role, we carbonate cementation is synchronous with pyritization; or propose a unifying model in which sedimentation rate was the (2) carbonate cementation follows dissipation of a lower pH primary factor controlling the pyritization–kerogenization microenvironment generated with BSR production of acidity. In gradient as observed in the Gaojiashan biota (Fig. 7). either case, no organic material remains or at least none is To help explain the model, we focus on four representative preserved through kerogenization. Regardless of which alternative preservational styles along the pyritization–kerogenization is more realistic, the true preservational distinction between gradient: (1) pervasive pyritization, (2) incomplete three- complete and incomplete three-dimensional pyritization hinges dimensional pyritization, (3) partial kerogenization with abun- on the duration, not the initiation, of pyrite formation. With dant pyrite association and (4) kerogenization with limited or regard to complete pyritization, we suggest that continuing pyrite highly diffuse pyrite association. For complete pyritization overgrowth is necessary for complete Conotubus tube infill, (Fig. 7a), initial pyrite mineralization must occur rapidly to whereas incompletely pyritized tubes instead are infilled with circumvent compression, and must continue to fill the entire carbonate cements after premature termination of pyritization. volume of the organism. If full pyritization occurs entirely in the At the other end of the Gaojiashan preservational spectrum are BSR zone, then the decaying carcass must stay in the BSR zone kerogenized carbonaceous compressions. While models for for a sufficient amount of time, requiring a thick BSR zone and/or kerogenization invoke the same facilitating taphonomic condi- a slow sedimentation rate following burial. The initial smothering tions for pyritization, three-dimensional structural rigidity is not event that entrapped the Conotubus organism rapidly placed it preserved, and instead organic tissues are stabilized to form below the oxic zone of aggressive aerobic decay, and subsequent geologically robust but two-dimensionally compressed carbonac- sedimentation proceeded sufficiently slowly to ensure a long eous remains. In the kerogenization taphonomic modes, enough duration in the BSR zone for complete pyritization. This pyritization is necessarily limited for tissues to be preserved as scenario is consistent with the d S data, with greater outer- carbonaceous compressions. The potential key is a rapid post- PY edge values suggesting an initial period of relatively rapid BSR, burial sedimentation rate and/or a narrower BSR zone, such that ensuring three-dimensional structural integrity, followed by a the fossilizing Conotubus tube is much more quickly moved progressive decrease in BSR rate (Supplementary Fig. 1) accom- through the BSR zone with little pyritization, thus positioning the panying greater isotopic fractionation and lower d S values. decaying organism within the methanogenesis zone shortly PY Volumetric considerations, however, suggest a shortage of following the onset of decay. In such a case, Conotubus tubes organic fuel from the Conotubus soft-tissue itself, which would that exhibit an appreciable amount of pyritization (Fig. 7c) may require either an exogenous source of carbon or production of have stayed in the BSR zone long enough to facilitate localized de novo organic carbon within the organic nucleus (for instance, pyritization but not extensively sustained for pyritization to by in situ chemoautotrophs) to continue fuelling further sulfide maintain three-dimensional structural integrity. Kerogenized production once the labile soft tissues of Conotubus were Conotubus with only diffuse pyrite (Fig. 7d) likely experience exhausted. Alternatively, pyritization could continue in the the majority of preservation within the methanogenesis zone methanogenesis zone where BSR is disfavoured but residual or during the earliest stages of decay, thus spending only very – 47 downward-diffusing porewater HS (or Fe–S complexes ) limited time in the BSR zone due to a high post-burial support pyrite overgrowth and continued pyritization. This sedimentation rate and/or a narrowed BSR zone. Following extended period of overgrowth may not show any clear textural these conditions, the fossil is predominantly comprised of change, but would obscure the anticipated U-shaped d S carbonaceous remains from kerogenization within the PY NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 9 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 methanogenesis zone. Methanogens are incapable of decompos- northwest margin of the Yangtze Platform (Supplementary Fig. 2A), the Gaojiashan region has numerous exposures of Ediacaran–Cambrian strata with ing higher molecular weight organic compounds, commonly broadly similar stratigraphy (from lower to upper): siliciclastic-dominated using acetate as the terminal electron acceptor (generalized: Doushantuo Formation; dolostone-dominated Dengying Formation; and – – CH COO þ H O-CH þ HCO ). If the breakdown of high- 3 2 4 3 phosphorite and carbonate of the basal Cambrian Kuanchuanpu Formation. molecular weight compounds via bacterial fermentation The Dengying Formation is tripartite (Supplementary Fig. 2B), consisting of – – (from lower to upper): thick-bedded, vuggy, peritidal dolostones of the (generalized: C H O þ4H O-2CH COO þ 2 HCO þ 4 6 12 6 2 3 3 þ B300-m-thick Algal Dolomite Member; thin-bedded calcareous siltstones, H þ4H ) is mostly limited to metabolically labile tissues, and mudstones and limestones of the B55-m-thick Gaojiashan Member that hosts aggressive aerobic degradation (generalized: CH COO þ O -2 3 2 the Gaojiashan Lagersta¨tte; and thick-bedded, vuggy, microbially laminated-to- – 48 CO þ H O þ OH ) was limited as a result of rapid burial, only stromatolitic, peritidal dolostone of the B200-m-thick Beiwan Member. 2 2 Correlation with the radiometrically dated Dengying Formation in the Yangtze the most recalcitrant structures such as the Conotubus tube walls Gorges suggests that the Gaojiashan Lagersta¨tte is constrained between 551 and will enter the fossil record. A few alternative scenarios should also 51,52 541 Myr ago . be considered. First, the Conotubus remains may indeed undergo Gaojiashan fossils mostly occur within millimetric beds of fine-grained degradation within the BSR zone, but instead occupy calcisiltite-siltstone of the Gaojiashan Member, interpreted to have been deposited microenvironments that are substantially limited in either or below storm wave base. Biostratinomic analysis of the Gaojiashan biota indicates that rapid event deposition played a key role in the exceptional preservation of both reactive iron or sulfate thus hindering pyrite precipitation. Gaojiashan fossils . The Gaojiashan biota is dominated by weakly biomineralized Second, the invocation of minimal ambient organic material for to non-biomineralized tubular and ribbon-like fossils (for example, Cloudina, pyritization may not hold in cases of kerogenization. That is, SRB Conotubus, Gaojiashania, Shaanxilithes and Sinotubulites), and also includes may prefer disseminated organic sources if Conotubus is protolagenid microfossils, algal debris, ichnofossils and microbial mat 11,28,53–59 textures . The focus of this study, Conotubus hemiannulatus, is currently emplaced within comparatively more organic-rich sediments, only known from the Gaojiashan Lagersta¨tte. Showing similarities in construction with Conotubus thus avoiding BSR-degradation and localized (Fig. 1d) and epibenthic life-mode, Conotubus has been interpreted as a possible 28,55 pyritization. Regardless, in either case, organic degradation is evolutionary precursor of Cloudina . Conotubus differs from Cloudina in its clearly limited to labile tissues, such that only the recalcitrant tube composition, as Conotubus was likely only weakly biomineralized at most . The fossiliferous unit occurs B18–49 m above the base of the Gaojiashan Member, tissues are eventually preserved as kerogens. with the Conotubus–dominated biofacies within the 26–39 m range corresponding Previous biostratinomical analysis of the late Ediacaran 13 18 60 to positive d C and negative d O excursions . Rare earth elemental Gaojiashan Lagersta¨tte has established that event deposits played geochemistry suggests that the Gaojiashan Member was deposited in a restricted an important role in the preservation of Gaojiashan fossils , but shallow sea environment, with riverine influx, common storm deposition influence , and high bioproductivity. the post-burial mineralization processes leading to the observed The samples studied herein were collected from calcareous siltstones 28–45 m pyritization–kerogenization gradient of preservation remain above the base of the Gaojiashan Member (Supplementary Fig. 2B). Three pyritized elusive. On the basis of geochemical analyses of three- Conotubus hemiannulatus specimens, collected 28–29 m above the base of the dimensionally pyritized Conotubus specimens, we have Gaojiashan Member (%1 in Supplementary Fig. 2B), were trimmed to sub-25-mm established that the pyritization process proceeded centripetally pieces, vacuum embedded in low-viscosity epoxy, and then ground and polished to make two longitudinal cross-sections and one transverse cross-section. These three from a rim of micrometric pyrite nucleated on the tube wall and specimens (reposited at the University of Missouri, Columbia; specimen numbers: fuelled by SRB degradation of labile tissues within the tube. This GJS-Cono001 to GJS-Cono003) were imaged and compositionally analysed using process can be described using a diffusion–precipitation scanning electron microscopy (SEM)/energy-dispersive X-ray spectroscopy (EDS). 31,32 34 model , modified to account for the role of an organic tube Sulfur isotopic compositions of pyrite (d S , reported as %-VCDT) were PY measured in situ using SIMS and on microdrilled powders using IRMS. A fourth in promoting the onset of pyritization by providing a preferable specimen, collected at 37–38 m above the base of the Gaojiashan Member (%3in substrate for nucleation. We suggest that preservation along the Supplementary Fig. 2B), on a larger slab was polished to make a transverse pyritization–kerogenization gradient can be understood as cross-section. This specimen (reposited at the Virginia Tech; specimen number: variations in the placement and duration of the carcass within 1GH2-70A) was analysed using SEM/EDS, ultraviolet photoluminescence microscopy and in situ X-ray diffraction (XRD). Both specimen number 1GH-70A the BSR and methanogenesis zones. The amount of time spent in and a non-fossiliferous slab, collected at 44–45 m above the base of the Gaojiashan each zone is principally influenced by post-burial sedimentation Member (%4 in Supplementary Fig. 2B), were microdrilled for IRMS d C and rate and/or BSR zone thickness, the latter of which is also related d O analyses (see Fig. 6a,b for drilling maps). An additional slab, collected 32 m to the availability of metabolizable organic material and sulfate. above the base of the Gaojiashan Member (%2 in Supplementary Fig. 2B), was analysed via IRMS for d S (data reported in Supplementary Table 1). The fossils that show three-dimensional pyritization, whether CAS pervasive or incomplete, spend more time in the BSR zone. In contrast, those that are two-dimensional carbonaceous Scanning electron microscopy. All SEM and EDS analyses (Fig. 2a–c,g; and Fig, 3a,c; Fig. 4a,b,e–g; Fig. 5b,e,f) were conducted using an FEI company Quanta compressions, either with extensive or diffuse pyrite association, 600 field-emission variable-pressure SEM with an integrated Bruker AXS Quantax are more rapidly buried in the methanogenesis zone. In each case, 400 high-speed silicon-drift EDS detector (Virginia Tech Institute for Critical degradation is required for preservation, and each mode may be Technology and Applied Science Nanoscale Characterization and Fabrication viewed as a complex balance between decay and mineralization. Laboratory). The specimens were analysed in high-vacuum mode (B6  10 Torr), B10 mm working distance, 20 keV beam accelerating voltage, 5.0 spot size These preservation processes, whether pyritization or (approximation of beam diameter and specimen current) and a system take-off kerogenization, are governed by the same suite of facilitating angle of 35 for EDS analyses. EDS point scans were conducted for 100 s live-time, taphonomic conditions, are primarily influenced by microbial and elemental maps were collected for 600 s live-time. decay pathways, and differ principally in the duration of interactions with the BSR and methanogenesis zones. Thus, the Secondary ion mass spectroscopy. All SIMS analyses followed d S methods PY scientific conversation regarding contributing factors of Beecher’s described in ref. 32, using a Cameca 7f GEO magnetic sector system (Virginia Tech Trilobite-type pyritization and Burgess Shale-type carbonaceous Institute for Critical Technology and Applied Science Nanoscale Characterization and Fabrication Laboratory). A Cs primary beam with 1 nA current at an energy compression should be shifted from facilitating factors such as a 32 34 49,50 18 of 20 kV was used to sputter the specimen, and the S and S isotopes were lack of bioturbation and bed-capping carbonate cements ,to detected using dual Faraday cup detectors from a B10 mm analytical spot. Mass those that drive mineralization and stabilization processes and are 32 16 resolution of B2,000 m per Dm was used to resolve the S from O mass directly responsible for fossil preservation. interference. A total of 214 spots across three specimens were analysed (Supplementary Table 1; Figs 2a,d–f; Fig. 3a,b; Fig. 4b–d), and measured d S PY values are reported as % deviation from VCDT (Vienna Canon Diablo Troilite; 34 32 Methods S/ S ¼ 0.0450045 ref. 61) calibrated via a Balmat pyrite standard 34 34 32 Materials. The Conotubus hemiannulatus specimens examined in this study were (d S ¼ 15.1%-VCDT; S/ S ¼ 0.04568407 refs 62,63). Each SIMS spot Balmat 34 32 collected from the Gaojiashan Member of the Dengying Formation at Gaojiashan measurement consisted of 10 cycles of S/ S ratios acquired from the same in Ningqiang county, southern Shaanxi Province, South China . Located in the physical spot after B2-min presputter to remove potential surface contamination. 10 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE The duration of individual spot analyses was B5 min, not including presputter. ´ 13. Farrell, U. C., Briggs, D. E. G., Hammarlund, E. H., Sperling, E. A. & Gaines, R. One-sigma errors of sample d S measurements were calculated from the PY R. Paleoredox and pyritization of soft-bodied fossils in the Ordovician instrumental standard error report of the 10 cycles, converted to %-VCDT. Frankfort Shale of New York. Am. J. Sci. 313, 452–489 (2013). 14. Raiswell, R. et al. Turbidite depositional influences on the diagenesis of Beecher’s Trilobite Bed and the Hunsruck Slate; sites of soft tissue pyritization. Ultraviolet photoluminescence and X-ray diffraction. Photoluminescence Am. J. Sci. 308, 105–129 (2008). microscopy and in situ XRD analyses were conducted on a UV microscope 15. Gaines, R. R. et al. Burgess shale  type biotas were not entirely burrowed away. (Olympus BX51) and a Rigaku Rapid II X-ray diffraction system with a 2D image Geology 40, 283–286 (2012). plate, in the S.W. Bailey X-ray Diffraction Laboratory, Department of Geoscience, 16. Orr, P. J., Briggs, D. E. G. & Kearns, S. L. Cambrian Burgess Shale animals University of Wisconsin. The polished cross-sectional slab of Conotubus, specimen replicated in clay minerals. Science 281, 1173–1175 (1998). number 1GH2-70A, was used in the analyses. All diffraction patterns were col- 17. Petrovich, R. Mechanisms of fossilization of the soft-bodied and lightly lected using reflection mode. Single-crystal diffraction patterns were also obtained armored faunas of the Burgess Shale and of some other classical localities. Am. to understand the crystallographic relationship between the dolomite and calcite in J. Sci. 301, 683–726 (2001). the zoned crystals (Fig. 5c,d,g). 18. Gaines, R. R. et al. Mechanism for Burgess Shale-type preservation. Proc. Natl Acad. Sci. USA 109, 5180–5184 (2012). 19. Butterfield, N. J. Does cement-induced sulfate limitation account for Burgess Isotope ratio mass spectroscopy. Carbon and oxygen IRMS analyses were Shale-type preservation? Proc. Natl Acad. Sci. USA 109, E1901 (2012). carried out at the University of Maryland and the Northwest University in Xi’an. 20. Xiao, S., Yuan, X., Steiner, M. & Knoll, A. H. Macroscopic carbonaceous Approximately 100 mg microdrilled powder was allowed to react for 10 min at compressions in a terminal Proterozoic shale: a systematic reassessment of the 90 C with anhydrous H PO in a Multiprep inlet system connected to an 3 4 Miaohe biota, South China. J. Paleontol. 76, 345–374 (2002). 13 18 Elementar Isoprime dual inlet mass spectrometer for d C and d O analysis. 21. Anderson, E. P., Schiffbauer, J. D. & Xiao, S. Taphonomic study of organic- Isotopic results are expressed in the standard d notation as % deviation from walled microfossils confirms the importance of clay minerals and pyrite in VPDB. Uncertainties determined by multiple measurements of NBS-19 were better Burgess Shale-type preservation. Geology 39, 643–646 (2011). than 0.05% (1s) for both C and O isotopes. 22. Gaines, R. R., Briggs, D. E. G. & Yuanlong, Z. Cambrian Burgess Shale–type Carbonate-associated sulfate sulfur IRMS analysis was carried out at Indiana deposits share a common mode of fossilization. Geology 36, 755–758 (2008). University. After trimming to remove visible veins and weathering rinds and 23. Van Roy, P. et al. Ordovician faunas of Burgess Shale type. Nature 465, ultrasonically cleaning in distilled deionized water, 56.3 g of whole rock was 215–218 (2010). crushed and pulverized into powder of o200 mesh size (74 mm) using a split- 24. Lin, J.-P. & Briggs, D. E. G. Burgess Shale-type preservation: a comparison of discus mill. Sulfate extraction followed the recommended protocol of ref. 64. Ultra- Naraoiids (Arthropoda) from three Cambrian localities. Palaios 25, 463–467 pure Milli-Q water (18 MO), purified NaCl, and distilled HCl were used to create (2010). solutions for leaching and acid digestion of the sample. The powder was immersed 25. Fike, D. A. & Grotzinger, J. P. A paired sulfate–pyrite d S approach to in 10% NaCl solution under constant magnetic stirring at room temperature until understanding the evolution of the Ediacaran–Cambrian sulfur cycle. Geochim. no sulfate was present in filtrate solutions. After water-leaching steps, the carbonate Cosmochim. Acta 72, 2636–2648 (2008). sample was dissolved in 10% HCl solution. The slurry was decanted and vacuum 26. Lin, S., Zhang, Y., Zhang, L., Tao, X. & Wang, M. Body and trace fossils of filtered through a 0.45-mm cellulose membrane filter. The acid-leached sulfate was metazoa and algal macrofossils from the upper Sinian Gaojiashan Formation in collected as BaSO by adding saturated BaCl solution. All collected BaSO samples 4 2 4 southern Shaanxi. Geol. Shaanxi 4, 9–17 (1986). were further purified by the DDARP method of ref. 65. BaSO was converted to SO using an Elemental Analyzer at 990 C and the d S measurement was 27. Farrell, U. C., Martin, M. J., Hagadorn, J. W., Whiteley, T. & Briggs, D. E. G. 2 CAS conducted on a Thermo-Electron Delta V Advantage mass spectrometer in Beyond Beecher’s Trilobite Bed: widespread pyritization of soft tissues in the continuous-flow mode. Late Ordovician Taconic foreland basin. Geology 37, 907–910 (2009). In addition, pyrite from samples GJS-Cono001 to GJS-Cono003 was 28. Cai, Y., Schiffbauer, J. D., Hua, H. & Xiao, S. Morphology and paleoecology of microdrilled and analysed for d S (s.d. ¼ 0.3%) to compare with SIMS PY the late Ediacaran tubular fossil Conotubus hemiannulatus from the Gaojiashan results. Pyrite extraction followed the chromium reduction method of ref. 66. Lagersta¨tte of southern Shaanxi Province, South China. Precambrian Res. 191, Sulfur isotopic results are expressed in the standard d notation as % deviation 46–57 (2011). from VCDT. 29. Bartels, C., Briggs, D. E. G. & Brassel, G. The Fossils of the Hunsru¨ck Slate: Marine Life in the Devonian 309 (Cambridge Univ. Press, 1998). 30. Bergstro¨m, J., Briggs, D. E. G., Dahl, E., Rolfe, W. D. I. & Stu¨rmer, W. Nahecaris References stuertzi, a phyllocarid crustacean from the Lower Devonian Hunsru¨ck Slate. 1. Cai, Y., Schiffbauer, J. D., Hua, H. & Xiao, S. Preservational modes in the Pala¨ontologische Zeitschrift 61, 273–298 (1987). Ediacaran Gaojiashan Lagersta¨tte: pyritization, aluminosilicification, and 31. Raiswell, R., Whaler, K., Dean, S., Coleman, M. L. & Briggs, D. E. G. A simple carbonaceous compression. Palaeogeogr. Palaeoclimatol. Palaeoecol. 326-328, three-dimensional model of diffusion-with-precipitation applied to localised pyrite formation in framboids, fossils and detrital iron minerals. Mar. Geol. 109–117 (2012). 2. Briggs, D. E. G. The role of decay and mineralization in the preservation of soft- 113, 89–100 (1993). bodied fossils. Annu. Rev. Earth Planet. Sci. 31, 275–301 (2003). 32. Xiao, S., Schiffbauer, J. D., McFadden, K. A. & Hunter, J. Petrographic and 3. Seilacher, A. Begriff and bedeutung der Fossil-Lagersta¨tten. N. Jb. Geol. SIMS pyrite sulfur isotope analyses of Ediacaran chert nodules: implications for Palaontol. Abh. 1970, 34–39 (1970). microbial processes in pyrite rim formation, silicification, and exceptional fossil 4. Allison, P. A. & Briggs, D. E. G. Exceptional fossils record: distribution of soft- preservation. Earth Planet. Sci. Lett. 297, 481–495 (2010). tissue preservation through the Phanerozoic. Geology 21, 527–530 (1993). 33. Berner, R. A. Sedimentary pyrite formation: an update. Geochim. Cosmochim. 5. Schiffbauer, J. D. & Laflamme, M. Lagersta¨tten through time: a collection of Acta 48, 605–615 (1984). exceptional preservational pathways from the terminal Proterozoic through 34. Wallace, A. F., De Yoreo, J. J. & Dove, P. M. Kinetics of silica nucleation on today. Palaios 27, 275–278 (2012). carboxyl- and amine-terminated surfaces: insights for biomineralization. J. Am. 6. Butterfield, N. J. Exceptional fossil preservation and the Cambrian Explosion. Chem. Soc. 131, 5244–5250 (2009). Integr. Comp. Biol. 43, 166–177 (2003). 35. Giuffre, A. J., Hamm, L. M., Han, N., De Yoreo, J. J. & Dove, P. M. 7. Xiao, S. & Schiffbauer, J. D. in From Fossils to Astrobiology: Cellular Origin, Life Polysaccharide chemistry regulates kinetics of calcite nucleation through in Extreme Habitats and Astrobiology (eds Seckbach, J. & Walsh, M.) 89–118 competition of interfacial energies. Proc. Natl Acad. Sci. USA 110, 9261–9266 (Springer, 2009). (2013). 8. Canfield, D. E. & Raiswell, R. in Taphonomy; releasing the data locked in the 36. Wood, T. L. & Garrels, R. M. Thermodynamic Values at Low Temperature for fossil record (eds Allison, Peter A. & Briggs, Derek E. G.) 337–387 (Plenum Natural Inorganic Materials (Oxford Univ. Press, 1987). Press, 1991). 37. Boudreau, B. P. & Canfield, D. E. A provisional diagenetic model for pH in 9. Briggs, D. E. G., Raiswell, R., Bottrell, S. H., Hatfield, D. & Bartels, C. Controls anoxic porewaters. J. Mar. Res. 46, 429–455 (1988). on the pyritization of exceptionally preserved fossils: an analysis of the Lower 38. Middelburg, J. J. A simple rate model for organic matter decomposition in Devonian Hunsrueck Slate of Germany. Am. J. Sci. 296, 633–663 (1996). marine sediments. Geochim. Cosmochim. Acta 53, 3581–3595 (1989). 10. Cai, Y. & Hua, H. Pyritization in the Gaojiashan Biota. Chinese Sci. Bull. 52, 39. Canfield, D. E. & Raiswell, R. in Taphonomy: Releasing the Data Locked in 645–650 (2007). the Fossil Record, Volume 9 of Topics in Geobiology (eds Allison, P. A. & 11. Cai, Y., Hua, H., Xiao, S., Schiffbauer, J. D. & Li, P. Biostratinomy of the late Briggs, D. E. G.) 411–453 (Plenum Press, 1991). Ediacaran pyritized Gaojiashan Lagersta¨tte from southern Shaanxi, South 40. Zhang, F., Yan, C., Teng, H., Roden, E. E. & Xu, H. In situ AFM observations of China: importance of event deposits. Palaios 25, 487–506 (2010). Ca-Mg carbonate crystallization catalyzed by dissolved sulfide: Implications for 12. Gabbott, S. E., Hou, X. G., Norry, M. J. & Siveter, D. J. Preservation of Early sedimentary dolomite formation. Geochim. Cosmochim. Acta 105, 44–55 Cambrian animals of the Chengjiang biota. Geology 32, 901–904 (2004). (2013). NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 11 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 41. Braissant, O. et al. Exopolymeric substances of sulfate-reducing bacteria: 62. Crowe, D. E. & Vaughan, R. G. Characterization and use of isotopically 34 32 Interactions with calcium at alkaline pH and implication for formation of homogeneous standards for in situ laser microprobe analysis of S/ S ratios. carbonate minerals. Geobiology 5, 401–411 (2007). Am. Mineral. 81, 187–193 (1996). 42. Habicht, K. S. & Canfield, D. E. Isotope fractionation by sulfatereducing natural 63. Kohn, M. J., Riciputi, L. R., Stakes, D. & Orange, D. L. Sulfur isotope variability populations and the isotopic composition of sulfide in marine sediments. in biogenic pyrites: reflections of heterogeneous bacterial colonization? Am. Geology 29, 555–558 (2001). Mineral. 83, 1454–1468 (1998). 43. Li, C. et al. A stratified redox model for the Ediacaran ocean. Science 328, 80–83 64. Wotte, T., Shields-Zhou, G. A. & Strauss, H. Carbonate-associated sulfate: (2010). experimental comparisons of common extraction methods and 44. Raiswell, R. & Berner, R. A. Pyrite and organic matter in Phanerozoic normal recommendations toward a standard analytical protocol. Chem. Geol. 326, marine shales. Geochim. Cosmochim. Acta 50, 1967–1976 (1986). 132–144 (2012). 45. Canfield, D. E., Raiswell, R. & Bottrell, S. H. The reactivity of sedimentary iron 65. Bao, H. Purifying barite for oxygen isotope measurement by dissolution and minerals toward sulfide. Am. J. Sci. 292, 659–683 (1992). reprecipitation in a chelating solution. Anal. Chem. 78, 304–309 (2006). 46. Berner, R. A. A new geochemical classification of sedimentary environments. 66. Canfield, D. E., Raiswell, R., Westrich, J. T., Reaves, C. M. & Berner, R. A. J. Sediment. Petrol. 51, 359–365 (1981). The use of chromium reduction in the analysis of reduced inorganic sulfur in 47. Rickard, D. & Luther, III G. W. Chemistry of iron sulfides. Chem. Rev. 107, sediments and shale. Chem. Geol. 54, 149–155 (1986). 514–562 (2007). 67. Froelich, P. N. Early oxidation of organic matter in pelagic sediments of the 48. Konhauser, K. O. Introduction to Geomicrobiology (Blackwell Publishing, 2007). eastern equitorial Atlantic: Suboxic diagenesis. Geochim. Cosmochim. Acta 43, 49. Allison, P. A. & Briggs, D. E. G. Burgess Shale biotas; burrowed away? Lethaia 1075–1090 (1979). 26, 184–185 (1993). 50. Orr, P. J., Benton, M. J. & Briggs, D. E. G. Post-Cambrian closure of the deep-water slope-basin taphonomic window. Geology 31, 769–772 (2003). Acknowledgements 51. Condon, D. et al. U-Pb ages from the Neoproterozoic Doushantuo Formation, This research was supported by funding through NASA Exobiology and Evolutionary China. Science 308, 95–98 (2005). Biology Program, NASA Astrobiology Institute (N07-5489), National Science Founda- 52. Bowring, S. A. et al. Geochronologic constraints on the chronostratgraphic tion (EAR-0824890, EAR095800, EAR1124062), Chinese Academy of Sciences, National framework of the Neoproterozoic Huqf Supergroup, Sultanate of Oman. Am. J. Natural Science Foundation of China (41202006; 41030209; 41272011), Chinese Ministry Sci. 307, 1097–1145 (2007). of Science and Technology, Virginia Tech Institute for Critical Technology and Applied 53. Cai, Y., Hua, H., Schiffbauer, J. D., Sun, B. & Xiao, S. Tube growth patterns and Sciences and China Postdoctoral Science Foundation (2013M531410). We would like to microbial mat-related lifestyles in the Ediacaran fossil Cloudina, Gaojiashan thank K.L. Shelton and J.W. Huntley for insightful discussion. Lagersta¨tte, South China. Gondwana Res. 25, 1008–1018 (2014). 54. Chen, Z., Bengtson, S., Zhou, C., Hua, H. & Yue, Z. Tube structure and original composition of Sinotubulites: Shelly fossils from the late Neoproterozoic in Author contributions southern Shaanxi, China. Lethaia 41, 37–45 (2008). J.D.S. designed the research with input from S.X. and Y.C. S.X. supervised the research. 55. Hua, H., Chen, Z. & Yuan, X. The advent of mineralized skeletons in J.D.S, S.X., Y.C. and H.H. performed the fieldwork. Sample preparation was performed Neoproterozoic Metazoa: new fossil evidence from the Gaojiashan Fauna. Geol. by J.D.S. and Y.C., SEM and EDS analysis was performed by J.D.S., SIMS analysis was J. 42, 263–279 (2007). performed by J.D.S. and J.H., ultraviolet and XRD analysis was performed by H.X., IRMS 56. Hua, H., Chen, Z., Yuan, X., Xiao, S. & Cai, Y. The earliest Foraminifera from analysis performed by Y.C., Y.P. and A.J.K. and geochemical data analysis was performed southern Shaanxi, China. Sci. China D 53, 1756–1764 (2010). by J.D.S., S.X. and A.F.W. J.D.S., with significant input from all of the authors, wrote the 57. Hua, H., Chen, Z., Yuan, X., Zhang, L. & Xiao, S. Skeletogenesis and asexual paper. reproduction in the earliest biomineralizing animal Cloudina. Geology 33, 277–280 (2005). Additional information 58. Hua, H., Pratt, B. R. & Zhang, L. Borings in Cloudina shells: complex predator- prey dynamics in the terminal Neoproterozoic. Palaios 18, 454–459 (2003). Supplementary Information accompanies this paper at http://www.nature.com/ 59. Meyer, M., Schiffbauer, J. D., Xiao, S., Cai, Y. & Hua, H. Taphonomy of the late naturecommunications Ediacaran enigmatic ribbon-like fossil Shaanxilithes. Palaios 27, 354–372 Competing financial interests: The authors declare no competing financial interests. (2012). 60. Zhang, P., Hua, H. & Liu, W. Isotopic and REE evidence for the Reprints and permission information is available online at http://npg.nature.com/ paleoenvironmental evolution of the late Ediacaran Dengying Section, reprintsandpermissions/ Ningqiang of Shaanxi Province, China. Precambrian. Res. 242, 96–111 (2014). 61. Ault, W. V. & Jensen, M. L. in Biogeochemistry of Sulfur Isotopes: National How to cite this article: Schiffbauer, J. D. et al. A unifying model for Neoproterozoic– Science Foundation Symposium Proceedings. (ed. Jensen, M. L.) 16–29 Palaeozoic exceptional fossil preservation through pyritization and carbonaceous (Yale Univ. Press, 1962). compression. Nat. Commun. 5:5754 doi: 10.1038/ncomms6754 (2014). 12 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Nature Communications Springer Journals

A unifying model for Neoproterozoic–Palaeozoic exceptional fossil preservation through pyritization and carbonaceous compression

Loading next page...
 
/lp/springer-journals/a-unifying-model-for-neoproterozoic-palaeozoic-exceptional-fossil-z3Lir04r0J

References (75)

Publisher
Springer Journals
Copyright
Copyright © 2014 by Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.
Subject
Science, Humanities and Social Sciences, multidisciplinary; Science, Humanities and Social Sciences, multidisciplinary; Science, multidisciplinary
eISSN
2041-1723
DOI
10.1038/ncomms6754
Publisher site
See Article on Publisher Site

Abstract

ARTICLE Received 28 May 2014 | Accepted 4 Nov 2014 | Published 17 Dec 2014 DOI: 10.1038/ncomms6754 A unifying model for Neoproterozoic–Palaeozoic exceptional fossil preservation through pyritization and carbonaceous compression 1 2 3 4 3 5 6 James D. Schiffbauer , Shuhai Xiao , Yaoping Cai , Adam F. Wallace , Hong Hua , Jerry Hunter , Huifang Xu , 7 8 Yongbo Peng & Alan J. Kaufman Soft-tissue fossils capture exquisite biological detail and provide our clearest views onto the rise of animals across the Ediacaran–Cambrian transition. The processes contributing to fossilization of soft tissues, however, have long been a subject of debate. The Ediacaran Gaojiashan biota displays soft-tissue preservational styles ranging from pervasive pyritization to carbonaceous compression, and thus provides an excellent opportunity to dissect the relationships between these taphonomic pathways. Here geochemical analyses of the Gao- jiashan fossil Conotubus hemiannulatus show that pyrite precipitation was fuelled by the degradation of labile tissues through bacterial sulfate reduction (BSR). Pyritization initiated with nucleation on recalcitrant tube walls, proceeded centripetally, decelerated with exhaustion of labile tissues and possibly continued beneath the BSR zone. We propose that pyritization and kerogenization are regulated principally by placement and duration of the decaying organism in different microbial zones of the sediment column, which hinge on post-burial sedimentation rate and/or microbial zone thickness. 1 2 Department of Geological Sciences, University of Missouri, Columbia, Missouri 65211, USA. Department of Geosciences, Virginia Tech, Blacksburg, Virginia 24061, USA. Early Life Institute, State Key Laboratory of Continental Dynamics, and Department of Geology, Northwest University, Xi’an 710069, China. 4 5 Department of Geological Sciences, University of Delaware, Newark, Delaware 19716, USA. Nanoscale Characterization and Fabrication Laboratory, Institute of Critical Technology and Applied Science, Virginia Tech, Blacksburg, Virginia 24061, USA. NASA Astrobiology Institute, Department of Geoscience, University of Wisconsin, Madison, Wisconsin 53706, USA. Department of Geological Sciences, Indiana University, Bloomington, Indiana 47405, USA. Department of Geology and Earth System Science Interdisciplinary Center, University of Maryland, College Park, Maryland 20742, USA. Correspondence and requests for materials should be addressed to J.D.S. (email: schiffbauerj@missouri.edu). NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 1 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 oft-tissue fossils in the geological record are rare relative to provide and locally concentrate necessary chemical constituents. the profusion of shelly hard parts. While shelly organisms Each case of soft-tissue preservation is thus a race between Sproduce mineralized structures in vivo, soft tissues require destructive decay and constructive mineralization processes . authigenic mineralization to enter the fossil record. The factors Superlative fossils occur in a narrow window where neither contributing to soft-tissue mineralization can be partitioned into degradation obliterates nor mineralization overprints important two distinct but complementary categories: those that facilitate biological details, a scenario contingent on both appropriate and those that drive preservation. Facilitating factors are typically settings and rapid stabilization processes. palaeoenvironmental in nature, serving to chemically or Spanning across the Ediacaran–Cambrian transition, when mechanically delay or inhibit aggressive aerobic degradation Konservat–Lagersta¨tten (deposits with exceptional soft-tissue 3 4,5 (noted in ref. 1 as ‘distal environmental and diagenetic preservation ) are most abundant , numerous mineralization 6,7 conditions’). While independently invoked as responsible for pathways fulfil the role of soft-tissue stabilizers . Two of these soft-tissue preservation, facilitating factors are neither mutually pathways—Beecher’s Trilobite-type pyritization (three- exclusive nor sufficient to guarantee fossilization. These dimensional pervasive pyritization) and Burgess Shale-type conditions can only enable soft-tissue preservation, because kerogenization (two-dimensional carbonaceous compression)— delaying degradation is only part of the preservational puzzle. are particularly important. Pervasive pyritization is commonly Driving factors refer to constructive mineralization processes that facilitated by rapid burial, minimal ambient organic material, replicate or stabilize soft tissues (‘proximal causes’ of ref. 1), periodic or persistent anoxia/dysoxia, reactive iron and sulfate ensuring their survivability through geological time and availability, low bioturbation and bacterial sulfate reduction 1,8–14  2– diagenetic alteration. Counterintuitively, many mineralization (BSR)-mediated decay (BSR: CH COO þ SO -2 3 4 – – processes are dependent on microbially mediated degradation to HCO þ HS ). By and large, kerogenization has been attributed to many of the same facilitating conditions, mostly related to rapid burial into anoxic/dysoxic palaeoenvironments . While a d numerous other palaeoenvironmental and diagenetic considerations have been invoked for kerogenization, such as 6,16 17 15,18 interactions with clays or ferrous iron , high alkalinity and oxidant restriction (that is, lack of sulfate for BSR) through early diagenetic sealing (though see also ref. 19), the common 1,6,12,16,20–24 association of kerogenized fossils with pyrite bolsters the interrelationship of these taphonomic processes. Fossils in the late Ediacaran (B551–541 Ma) Gaojiashan Lagersta¨tte illustrate a preservational gradient from pervasive pyritization to compressed kerogenization , including three- dimensional pervasive pyritization, incomplete pyritization and carbonaceous compression with associated pyritization. As such, this Lagersta¨tte offers an opportunity to establish a comprehensive taphonomic model marrying these pathways. To this end, we geochemically investigate the abundant Gaojiashan fossil Conotubus hemiannulatus, which shows preservation in each of these taphonomic styles. Our data form the basis for the proposed unifying model, which invokes sedimentation rate, and Py Ca cement thus time the decaying carcass spends in specific microbial zones, to regulate taphonomic styles along the pyritization–kerogeni- zation gradient. Results General taphonomic observations. Among hundreds of Con- otubus specimens examined in this study, B80% are preserved three-dimensionally through complete or incomplete pyritization (Fig. 1a,b), with the remaining preserved through two-dimen- sional kerogenization (Fig. 1c). Pervasively pyritized Conotubus specimens possess secondary cracks filled with calcite cements, and thin rinds (o20mm) of iron oxide along these cracks (Figs 2g,3c and 4e). Viewed in longitudinal and transverse cross- sections (Figs 2a,3a and 4b), these specimens show a bimodal size distribution of pyrite crystals. Generally, a micrometric size class Figure 1 | Taphonomic representations of Conotubus hemiannulatus. of crystals ranges from B10 to B250mm, and a millimetric size (a) Pervasively pyritized (rusty weathered colour) Conotubus on bedding class of crystals ranges from B800mm to a few mm. Micrometric plane. Scale bar, 5 mm. (b) Longitudinally fractured Conotubus specimen pyrite crystals are mainly found at the outer edge of the fossil showing carbonate cement infill (labelled Ca cement), with pyritized (Figs 2a and 3a) and sometimes along non-continuous central (labelled Py) nested funnel walls visible (arrows). Scale bar, 1 mm. voids (Fig. 3a) or fractures (Figs 2a and 4b), whereas millimetric (c) Specimen of Conotubus preserved as two-dimensional carbonaceous pyrite crystals comprise the bulk of the tube interior (Fig. 2a). In compressions with aluminosilicate coating. Scale bar, 5 mm. (d) Interpretive some cases, millimetric crystals appear to be amalgamations of schematic of Conotubus showing flexible, funnel-in-funnel tube structure micrometric crystals (Fig. 3a). In others, millimetric crystals and morphology. Figures in b,c are reproduced with permission from appear to have subtle textural variations along their outer edges, Elsevier (modified from ref. 28 and ref. 1, respectively). possibly indicative of later overgrowth (Fig. 2b,c). 2 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. Frequency (%) NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE >–19 ‰ Left transverse transect Right transverse transect ade 5 35 –19 to <–21 ‰ Mean = –28.3‰ Mean = –24.0‰ –21 to <–23 ‰ –23 to <–25 ‰ –25 to <–27 ‰ 4 –27 to <–29 ‰ –29 to <–31 ‰ –31 to <–33 ‰ 3 ≤–33 ‰ bc –40 –30 –20 –10 –40 –30 –20 –10 δ S (‰-VCDT) Longitudinal transect Frequency (%) g 0 5 15 25 Mean = –25.5‰ 35 –10 –20 –30 –40 012 3456789 Point position (mm) FeS -Fe-Ca-Si Figure 2 | SEM/EDS and SIMS d S data for Conotubus specimen GJS-Cono001. (a) Backscatter Z-contrast electron micrograph montage of PY longitudinal section, with all SIMS spots (circles) plotted at analysis location. Microdrilling location for IRMS d S assessment indicated by star. Point PY and star colour corresponds to d S bins shown in upper left key. Scale bar, 1 mm. Insets (b,c) at lower left show higher magnification split-frame of PY black rectangle region highlighting subtle textural difference associated with pyrite overgrowth (arrows in each panel); backscatter electron (b) and secondary electron (c) images. Scale bar, 250mm. (d–f) SIMS transects, with dashed lines indicating mean values and histograms showing frequency of points by 1% bins. Note generalized U-shaped profile in d (left transect), with higher values towards fossil edges and lower values centrally located. To show precision of each 10-cycle point sample mean, error bars mark 1 standard error. These errors do not include the analytical uncertainties of the Balmat pyrite standard, which are relatively small. (g) Energy-dispersive X-ray elemental overlay of iron-sulfur (gold), iron but no sulfur (red), calcium (blue) and silicon (green). Map region corresponds to red rectangle in a. Scale bar, 500mm. Transverse transect > –19 ‰ a b Mean = –28.8‰ 4 35 –19 to <–21 ‰ –21 to <–23 ‰ –23 to <–25 ‰ –25 to <–27 ‰ –27 to <–29 ‰ –29 to <–31 ‰ –31 to <–33 ‰ ≤–33 ‰ –40 –30 –20 –10 0 δ S (‰-VCDT) FeS -Fe-Ca-Si Figure 3 | SEM/EDS and SIMS d S data for Conotubus specimen GJS-Cono002. (a) Backscatter Z-contrast electron micrograph montage of PY longitudinal section, with all SIMS spots (circles) plotted at analysis location. Microdrilling location for IRMS d S assessment indicated by star. PY Point and star colour corresponds to d S bins shown in upper left key. Scale bar, 1 mm. (b) SIMS transect, with dashed line indicating mean value, PY and histogram showing frequency of points by 1% bins. To show precision of each 10-cycle point sample mean, error bars mark 1 s.e. These errors do not include the analytical uncertainties of the Balmat pyrite standard, which are relatively small. (c) EDS elemental overlay of iron-sulfur (gold), iron but no sulfur (red), calcium (blue) and silicon (green). Map region corresponds to red rectangle in a. Scale bar, 500mm. NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 3 & 2014 Macmillan Publishers Limited. All rights reserved. δ S (‰-VCDT) Point position (mm) Point position (mm) Frequency (%) ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 –19 to <–21 ‰ ab –21 to <–23 ‰ –23 to <–25 ‰ –25 to <–27 ‰ –27 to <–29 ‰ –29 to <–31 ‰ Frequency (%) cd 0 5 15 25 35 0 5 15 25 35 –10 Diameter Circumference Mean = –21.8‰ Mean = –25.2‰ –20 –30 –40 012345 01 Point position (mm) ef g FeS -Fe Si 2 Ca Figure 4 | SEM/EDS and d S data for Conotubus specimen GJS-Cono003. (a,b) Backscatter Z-contrast electron micrograph montage of transverse PY section, with all SIMS spots (circles) plotted at analysis location. Microdrilling for IRMS d S was made on the reverse side of the specimen at a location PY corresponding to the star. Point and star colour corresponds to d S bins shown in upper right key. Scale bar in a, 2 mm, in b, 500mm. (c,d) SIMS PY circumference and diameter transects, respectively, with dashed lines indicating mean values, and histograms showing frequency of points by 1% bins. 34 34 Circumference d S plot follows clockwise from straight arrow in b. Using dashed red line in b as a reference, note slight separation of d S values: PY PY 34 34 34 higher d S values to the right and lower d S values to the left of the dashed line in b. Diameter d S plot follows top-to-bottom. To show the PY PY PY precision of each 10-cycle point sample mean, error bars mark 1 s.e. These errors do not include the analytical uncertainties of the Balmat pyrite standard, which are relatively small. (e–g) EDS elemental overlay of iron-sulfur (gold), iron but no sulfur (red), calcium (blue) and silicon (green). Map region corresponds to red rectangle in a. Scale bar in g is 500mm, applicable for e and f. Sulfur isotopic data. Pyrite sulfur isotopic values (d S ), Carbon and oxygen isotopic data. Three-dimensionally but PY measured using secondary ion mass spectroscopy (SIMS), range incompletely pyritized Conotubus specimens show an outer rim between –7.6 and –37.9%-VCDT (Supplementary Table 1 and of pyrite, with multiple generations of compositionally distinct Fig. 2a,d–f; Fig. 3a,b; Fig. 4b–d). Although not a hard-and-fast carbonate cements surrounding a central void in the tube interior rule, pyrite with d S values Z–19% tend to be associated with (Fig. 5). In the only chemically analysed cross-section with this PY fractures and/or textural variations in the pyritized fossil, which preservational style but representative of other similarly preserved may correspond to later overgrowth (for instance, see adjacent specimens, the outer first generation cements consist of large red points in Fig. 2a longitudinal transect positioned just below centripetally terminating calcite crystals, indicating inward car- arrows indicating textural variation in Fig. 2b,c). Disregarding bonate growth from the pyrite rim. The inner second generation obvious fracture-associated S-enriched points, the transverse cements are zoned rhombohedral crystals, with alternating d S transects exhibit a generalized U-shaped profile, with ultraviolet-luminescent zones of ferroan dolomite and dull zones PY localization of greater values along the tube-wall edges and lower of dolomite þ calcite. Carbon and oxygen isotopic compositions values towards the center of the fossil (Fig. 2d,e). This pattern is of microlaminae in the host rock and for the two generations of not discernable in all specimens (Figs 3b and 4c,d). Microdrilled fossil carbonate cements were determined (Supplementary pyrite assessed via isotope ratio mass spectroscopy (IRMS) Table 2 and Fig. 6). The mean d Cvalue of the darker coloured yield d S values broadly similar to mean SIMS values microlaminae (6.1 0.9% VPDB) is greater than that of the PY (Supplementary Table 1). Carbonate-associated sulfate sulfur lighter coloured microlaminae (4.4 1.0%) with slight overlap in 34 18 isotopic composition (d S ) of host rock was assessed at ranges, whereas their mean d O values are broadly similar CAS þ 33.6%-VCDT (Supplementary Table 1), comparable to con- (darker microlaminae ¼ –5.4 1.2%; lighter microlaminae ¼ 25 34 temporaneous units in Oman . Thus, D S is appreciably –5.9 0.3%) with mostly overlapping ranges. While similar in CAS-PY high (ranging from þ 41.2 to 71.5%). carbon isotope composition, the cements in the Conotubus 4 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. δ S (‰-VCDT) NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE ab Host rock Laminae CV IC Py rim OC e f Ca-Mg Fe-Si Calcite Dolomite Light laminae Dark laminae Outer cement Inner cement 10 15 20 25 30 Diffraction angle, 2 (degrees) Figure 5 | Ultraviolet photoluminescence and in situ XRD data for Conotubus specimen 1GH2-70A. (a) Overview photomicrograph of transverse slab of Conotubus and surrounding matrix of laminated rock. Note pyrite or iron oxide rim (gold colour), outer carbonate cement (dark colour), inner carbonate cement (light colour) and central void. Scale bar, 10 mm. (b) Backscattered Z-contrast electron micrograph montage of region defined by white rectangle in a. Fine pyrite or iron oxide rim (Py rim) seen as bright discontinuous specks, surrounding carbonate cements (IC: inner cement; OC: outer cement) and central void (CV). Scale bar, 1 mm. (c) Ultraviolet photoluminescence microscopy of black rectangle region in a, showing zoned carbonate crystals in inner cement. Scale bar, 1 mm. Inset (d) shows higher magnification view of white rectangle in c for better detail of crystal zoning. Scale bar, 500mm. (e,f) EDS elemental maps of white rectangle region in b, with calcium (orange) and magnesium (green) overlay shown in e and iron (red) and silicon (blue) overlay shown in f. Scale bar in f is 1 mm, applicable for e.(g) In situ XRD patterns of host rock light- and dark-coloured laminae, outer carbonate cement within fossil and inner carbonate cement within fossil. Characteristic peak positions of calcite and dolomite are shown in orange and green vertical dashed lines, respectively. The strongest diffraction peaks from calcite and dolomite are labelled with C and D , respectively. tube and the host rock have distinct d O values. Between Discussion fossil-interior cement generations, the outer calcite cements have Previous analyses of pyritized Palaeozoic Lagersta¨tten suggest 13 18 13 slightly greater mean d C and d O values (d C ¼ 6.1 0.1%, rapid burial into anoxic sediments, which in turn reduces d O ¼ –8.2 0.2%) than the inner dolomite þ calcite cements bioturbation, impedes organic deterioration and emplaces the 13 18 ± ± (d C ¼ 5.2 0.4%, d O ¼ –9.0 0.2%). decaying carcasses within the sulfidic BSR zone below the oxic-anoxic boundary in the sediment profile. Further, pyritization-conducive sediments typically have low organic Compaction. Three-dimensional preservation of Conotubus carbon content and abundant reactive iron, serving to focus 8,9,13,14,27 BSR and pyrite precipitation on decaying carcasses . allows an estimate of the compaction ratio of the host sediments. Viewed perpendicular to bedding plane, the calcisiltite/calcilutite While the Gaojiashan biota is similar to these younger deposits in that pyritized fossils are found in sediments deposited by microlaminae warp around nearly circular Conotubus tubes (Figs 4a,b,5 and 6). Measurements of microlaminae surrounding rapid burial events , there are some key differences. First, the full pyritization–kerogenization preservational gradient from Conotubus tubes in comparison with their thickness extending beyond the fossil yields an estimated sediment compaction ratio three-dimensional pervasive pyritization to two-dimensional of B1.85:1. Conotubus tubes show negligible compaction, with a kerogenized compressions, with intermediate or admixed major:minor axis ratio of B1.15:1, although an oblate cross- preservational modes, appears to be unique to the Gaojiashan section may be biological . Lagersta¨tte. Second, the tubular fossils of the Gaojiashan biota NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 5 & 2014 Macmillan Publishers Limited. All rights reserved. Relative intensity 104 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 a b Light-coloured lamina below fossil (a) c Light-coloured lamina above fossil (a) Dark-coloured lamina (a) Light-dark laminae (b) Outer cement within conotubus (a) Inner cement within conotubus (a) –9.5 –8.5 –7.5 –6.5 –5.5 –4.5 –3.5 –2.5 δ O (‰-VPDB) 13 18 Figure 6 | Host rock and fossil carbonate IRMS d C and d O data. (a) Microdrill map of slab 1GH2-70A with Conotubus specimen. Scale bar, 13 18 10 mm. (b) Microdrill map of slab (two continuous pieces) without Conotubus fossils. Scale bar, 50 mm. (c) Cross-plot of all d C and d O analyses. Convex hulls and nested convex hulls (shaded) show groupings of data by location of microsampling. Yellow points show light-coloured laminae (single circle below fossil and double circle above fossil in a; dashed circle from slab in b). Blue points show dark-coloured laminae (single circle contiguous to fossil in a; dashed circle from slab in b). Red and green diamonds show outer and inner cements in a, respectively. Keys also applicable for microdrill location maps. 10,28 notably do not retain their most labile soft parts , showing no porewaters with respect to iron sulfide at some distance from the evidence of the soft-bodied organisms that lived within these organic nucleus. The spatial trends in both pyrite crystal tubes. While some sites of pervasive pyritization show glimpses of morphology and d S values of Conotubus fossils are PY highly labile soft-tissue preservation, such as pygnogonid and consistent with centripetal pyrite growth controlled by the 29,30 31 crustacean musculature from the Hu¨nsruck Slate , pervasive diffusion–precipitation dynamics of mineralization . Similar to pyritization of Conotubus only captures the three-dimensional the formation of pyrite rims around chert nodules and 8,31 exterior morphologies of the tubes. The original histology of carbonate concretions , sulfate reducing bacteria (SRB) Conotubus tubes is unknown. However, they have been metabolized a centrally located organic nucleus, in this case the interpreted as supportive, refractory tissues, either non- labile tissues of the Conotubus organism, generating an outward biomineralized or weakly biomineralized . diffusion of sulfide. The sulfide meets with an inward-diffusing Building upon the Raiswell et al. diffusion–precipitation reactive iron sourced from ambient porewater, forming a reaction model for pyritization, we can begin to elucidate the progression front where pyrite-precursor iron monosulfide precipitation of pervasive fossil pyritization and provide insights into early occurs. As this process proceeds, the organic nucleus is diagenetic conditions responsible for the taphonomic styles progressively exhausted, resulting in an inward shift in the observed in the Gaojiashan Lagersta¨tte. According to this reaction front (Supplementary Fig. 1). model , the locus of mineralization is controlled by the One complicating issue, however, is that the recalcitrant tube intersection of two diffusion fields. The first arises as a walls of Conotubus would form a barrier to impede but not consequence of BSR, driving sulfide outward into the sediment entirely halt diffusion, resulting in accumulation of sulfide and porewaters. The second originates from sediment sources, reactive iron on either side of the tube walls. As such, we must carrying reactive iron toward the decaying organic nucleus. The consider another important factor controlling the locus of intersection of these two diffusion fronts results in supersaturated pyritization: heterogeneous nucleation facilitated by an organic 6 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. δ C (‰-VPDB) Sedimentation rate NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE Pervasive pyritization Incomplete pyritization Partial kerogenization/pyritization Diffuse pyrite kerogenization a b c d Sediment–water interface Aerobic NO NO 2+ 2+ Mn Mn Fe/Mn/DN 2– SO SO 2+ 2+ Fe Fe Termination of HS HS Limited pyritization BSR pyritization Kerog. F Fe-S e-S Kerogenization BSR BSR pyritization Carbonate infill comple complex xes es Pyrite overgrowth C CH H Methanogenesis Time Rapid event burial 0 1 2 3 4 10 10 10 10 10 Background sedimentation Conc. (μM) Figure 7 | Pyritization–kerogenization taphonomic gradient. Fossil examples (a–d, upper panels) and proposed taphonomic model (lower panels) with sedimentary microbial zonation. Diagonal lines track the position of the decaying organisms in the sediment column, and the slope of each line represents sedimentation rate. Grey upper diagonal line corresponds to rapid event burial, and black lower diagonal line corresponds to post-burial sedimentation. Brackets indicate the length of time the decaying organism resides in the BSR zone (gold colour), and experiences BSR-mediated pyrite growth, although pyrite overgrowth may continue into underlying methanogenesis zone (blue colour). From left to right, each diagram indicates a shortened residence time in the BSR zone as compared with the previous panel, which could result from either, or both, changes in post-burial sedimentation rate and BSR zone thickness. (a) Pervasively pyritized Conotubus in transverse cross section. Scale bar, 2.5 mm. Diagram shows initial rapid event deposition, followed by slow post-burial sedimentation. (b) Polished transverse cross-section of pyritized Conotubus showing carbonate in the center and thin outer lamina (arrow) representing nested tube wall. Scale bar, 1 mm. Corresponding diagram shows increase in post-burial sedimentation rate and reduction in BSR zone thickness, leading to comparatively earlier termination of pyritization. (c) Specimen of Conotubus with admixed taphonomic mode of pyritization (black arrows) and carbonaceous compression (white arrows). Scale bar, 5 mm. Diagram shows further increase in post-burial sedimentation rate and reduction in BSR zone thickness, yielding partial pyritization and onset of kerogenization once carcass exits BSR zone. (d) Specimen of Conotubus preserved via complete kerogenization with diffuse pyrite. Scale bar, 5 mm. Diagram shows highest post-burial sedimentation rate and thinnest BSR zone, with limited pyritization, and earliest onset of kerogenization. Relative abundances of chemical species at right follows that of refs 47,48 after ref 67. Fe–S complexes – 2 þ curve shows possible continued pyrite overgrowth from downward diffusion of HS /Fe . Figures in a–d are reproduced with permission from Elsevier (modified from ref. 1 and ref. 28). substrate. The individually conserved nested Conotubus tube matrices , significant variations in the surface nucleation rate walls (Figs 1b and 7b) may have promoted pyritization by may occur between biopolymers with similar functionalities, with providing a naturally favourable substrate for the initiation of the specific order of substrate preference depending chiefly on iron sulfide nucleation—an unaccounted-for factor in the supersaturation. traditional model . During the earliest stages of microbially induced degradation, The ability of an organic substrate, such as the tube walls, to when nucleation sites on the tube surface are most abundant, promote mineralization can be readily justified within the pyritization is dominated by precipitation of abundant micro- constructs of classical nucleation theory. For a cube-shaped metric crystals as are observed at the outer edges of the nucleus, the relationship between the free energy barrier opposing Conotubus specimens. The size and location of the crystallites the formation of a stable nucleus in solution (homogeneous case) indicates that the organic tube-wall surface likely plays a role in het and on a foreign substrate is: DG ¼ DG ð Þ, where a directing the onset of nucleation, and that the pyrite super- hom het hom 2a hom and a are the interfacial energies of the homogeneous and saturation state, s, was relatively high as compared with the later het heterogeneous nuclei. Although a depends on the balance stages of mineralization when pyritization proceeds through het between the liquid-nucleus, liquid-substrate and substrate- coarsening of existing crystals rather than formation of new nucleus interfacial tensions, a simple analysis shows that if crystals. This interpretation is supported by the nucleation rate DG =k T  B=s a Ea , the free energy barrier opposing nucleation at a equation, J ¼ Ae ¼ Ae , where A is a pre- hom het n surface is reduced to half of the homogeneous barrier. As exponential constant (whose units represent the number of nucleation rate shows an exponential dependence on DG*, this molecules attaching to a critically-sized nucleus per unit time and translates into a substantial increase in the rate of surface surface area), B is a constant that describes the shape of the nucleation. Indeed, nucleation rates depend strongly on the nucleus, T is temperature, k is the Boltzmann constant, DG* is chemical nature and physical structure of the organic interface. free energy matching the thermodynamic barrier opposing ion activity product For instance, NH terminated surfaces can be completely passive nucleation and s is supersaturation ðln Þ. This solubility product to the formation of amorphous SiO ; however, under identical equation shows that an increase in supersaturation state generally þ – conditions, NH /COO surfaces promote SiO deposition to the results in a higher number of nuclei per unit area of substrate or 3 2 extent that the organic may be coated by a nearly-coherent volume of solution in the case of homogeneous nucleation. As nanoscale layer of amorphous material within a few hours . compared with any soft body tissues of the Conotubus organism, Moreover, as evidenced by calcite nucleation on polysaccharide the tube walls must have provided the most chemically favourable NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 7 & 2014 Macmillan Publishers Limited. All rights reserved. Microbial zonation with sediment depth ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 32,39 13 nucleation sites for initiation of pyrite growth. Pyrite crystals in precipitation . While similar relatively heavy d C values of these regions are isotopically heavier (d S typically 4–25%; host rock and fossil cement render BSR- or BFeR-sourced PY bicarbonate as insignificant contributors, dissolved sulfide is Fig. 2a,d,e) than those in the tube interior, indicating a progressive decline in BSR rate throughout the pyritization observed to enhance crystallization of calcite and dolomite , process and corresponding relaxation in diffusion-limited sulfate possibly contributing to early calcite cementation. In addition, availability. The inferred sulfate limitation in initial pyritization SRB exopolysaccharides commonly incorporate metal cations may seem contradictory to the high D S values (such as Mg and Fe), which could facilitate precipitation of high- CAS-PY (Supplementary Note 1). However, oxidative recycling of sulfide Mg calcite and ankerite . The B2% difference between 14 18 and oxidation of detrital pyrite entrained in microturbidites carbonate cement d O values within the Conotubus specimen 34 13 likely supplied S-depleted sulfate for pyritization, thereby and host carbonates, but broadly similar d C values (Fig. 6c), contributing to the high D S values. As BSR continues suggest that the cements may have been slightly influenced by CAS-PY over time, labile tissues are diminished and BSR necessarily slows diagenetic fluids without significant alteration of carbon isotopic 18 13 because of decreasing availability of metabolizable organic carbon composition. Slightly lower d O and d C values in the inner rather than sulfate exhaustion or deep burial, which would versus outer cements indicates a stronger influence of diagenetic instead yield a shift towards higher d S values. As a result of fluids on the inner cementation, consistent with petrographic PY slowed BSR, sulfide production rate would drop, supersaturation evidence showing a later origin than the outer cements. The levels with respect to iron sulfide would decrease and nucleation relatively small isotopic difference between the cements and would be disfavoured. Thus, iron sulfide precipitation is focused sedimentary matrix suggests that carbonate cementation may on overgrowing existing crystals, leading to the formation of have occurred shortly after the cessation of pyritization, playing a millimetric crystals. During this shift, d S values would constructive preservational role by enhancing the rigidity of PY decrease as the BSR system switches from sulfate limitation to partially pyritized tubes before sediment compaction. organic limitation. The expected result is a U-shaped d S While we have established that both pervasive and incomplete PY profile as observed in some specimens (Fig. 2d,e), although this pyritization must have predated sediment compaction based on profile can be obscured by pyrite overgrowth (see Discussion warping host rock microlaminae encasing the Conotubus fossils, below). we can further constrain the duration of the pyritization process. From the understanding of how the pyritization process To do so, we must consider requisite levels of sulfate, reactive iron proceeds and expectations for resultant sulfur isotopic trends and metabolizable organic material. On the basis of the size of (Supplementary Note 1), we can then shift our focus to resolving Conotubus specimens, with a maximum diameter of 12 mm and the geochemical constraints for pervasive pyritization. With the length of 3–80 mm (ref. 28), the amount of sulfate required for 7 þ Vr first dissociation constant of H S at 1.05  10 (K ¼ [H ] complete pyritization will follow M ¼ 2 , where V is the 2 1 0 sulfate pyrite [HS ]/[H S]) and seawater pH typically constrained to B7.5–8.5, volume of the Conotubus tube, r is the density of pyrite (E5 g per HS is the dominant dissolved sulfide species. Thus, we can write 3  1 cm ) and M is the molar mass of pyrite (E 120 g mol ). 2 þ 0 – þ pyrite the precipitation of pyrite as Fe þ S þ HS -FeS þ H , Using V ¼ p*r *l for the volume of a cylinder, with Conotubus such that the equilibrium solubility product for pyrite is given as radius (r) and length (l) simplified as 5 and 40 mm, the total 2 þ   pH  16.35 K ¼ [Fe ][HS ]/10 ¼ 10 (ref. 36). With activity sp sulfate required is 0.26 moles. The amount of reactive iron needed – 2 þ coefficients for HS and Fe in seawater at 0.67 and 0.26 is 0.13 moles. The amount of organic carbon needed varies by the (ref. 37), we can then calculate the apparent solubility product for electron donor compound used (largely fermentative end pH K ð10 Þ sp 2 0  24 pyrite as K ¼ ¼ 8:110 ðM Þ at the low end of HS products; Supplementary Table 3). For simplicity, we use BSR sp g g 2 þ Fe normal seawater pH. As such, given the Raiswell et al. model of acetate, which, in accordance with the above constraints, requires 0.52 moles of organic C. If we then assume that the assumption of the estimated ratio of reservoir concentrations (C ) 0 0 2 þ – of sulfur to iron, C :C o0.1 (that is, [Fe ]Z10  [HS ]), for interior volume of Conotubus tube is completely full of soft tissue S Fe (an overestimate), with a nested tube-wall thickness of 1 mm localized pyrite formation at the site of decay , reactive iron must be greater than approximately 9  10 M to drive pyrite (Fig. 1b), the volume of soft tissue that contains metabolizable organic material using the same dimensions as above is B2cm . precipitation, well below modern observations of anoxic Assuming that the soft tissue was pure amorphous carbon sediments ato10 M (refs 8,31). Because the majority of the ¨ (density ¼B1.8 g cm ), 0.52 moles would occupy a volume of fossils in the Gaojiashan Lagerstatte exhibit three-dimensional B3.5 cm , a substantially larger volume than is available within pervasive pyritization , we can surmise an excess of available the Conotubus tube. As such, given realistic carbon contents in sediment/porewater reactive iron. Assuming a decay constant animal tissues, we can deduce that there is a deficit of endogenous of 0.1–1.0 per year (reported for organic decay in marine sediments ) and an organic nucleus radius of 0.1–1.0 cm carbon to account for the volume of pyrite precipitated—which is clearly problematic, but disregarded for now and revisited in our (appropriate for Conotubus with a maximum diameter of 1.2 cm (ref. 28)), porewater dissolved sulfide concentrations of model description below. On the basis of these calculations and high-end rates of sulfate reduction in Ediacaran sediments o10 M are required for soft tissue pyritization (Fig. 3 in ref. 31). As localized pyritization of highly labile tissues occurs when (6.935 mmol cm per year according to ref. 42, with pervasive 0 0 2 þ anoxic conditions and higher metabolizability of organics before C :C o0.1 (ref. 31), Fe content in porewater may have been S Fe 32,42–44 3 2 þ up to 10 M. We can thus reasonably constrain porewater Fe the evolution of vascular plants ), we can calculate an 12 – approximate timeframe for generating sufficient HS to content in Gaojiashan sediments between 9  10 M and 10 M, justified by the lack of labile soft-tissue pyritization in pervasively pyritize a Conotubus tube with a 3.14 cm total volume. If the 0.26 moles of SO is derived entirely this Lagersta¨tte. endogenously within a Conotubus tube, a total of 82.8 mmol In incompletely pyritized but three-dimensional Conotubus – 3 HS per cm is required for pyritizing the full volume of the tube. tubes, alkalinity generated during BSR (Supplementary Table 3) At a rate of 6.935 mmol cm per year, a total of B12 years and bacterial Fe(III) reduction (BFeR: CH COO þ 2 þ – 8 Fe(OH) -2 HCO þ8Fe þ 15 OH þ5H O) could would be required to generate enough HS for pyritization. Even 3 3 2 at modern rates of sulfate reduction, such as measured rates of contribute to carbonate infill assuming appropriately basic microenvironmental pH levels to facilitate calcite 0.1 mmol cm per year (ref. 45), this yields 828 years to generate 8 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE – – 34 enough HS for pyritization of moderately sized Conotubus tubes. profile because residual porewater HS tends to have greater d S The decaying organism is a BSR hotspot, which should pull in values. In combination, the observed subtle textural variations 2– 2 þ 34 both SO and Fe from the surrounding microenvironment (Fig. 2b,c) and higher d S values along millimetric crystal 4 PY (as opposed to assumed steady-state equilibrium ), thus these edges may support this alternative scenario. Regardless, the keys cited bulk-sediment rates may overestimate the pyritization time. for complete pyritization are rapid burial and initial pyritization It is important to note, however, that these estimates assume that to maintain structural integrity, followed by prolonged pyrite HS is: (1) a rate-limiting factor for pyrite precipitation and (2) overgrowth within and perhaps below a relatively thick BSR zone entirely derived from BSR in and around the decaying Conotubus to completely fill Conotubus tubes with pyrite. organism in the BSR zone. As discussed below, these assumptions Incomplete but three-dimensional pyritization (Fig. 7b) may not be valid. requires the same facilitating taphonomic conditions as complete From these and previously reported observations , the data pyritization, including rapid placement in the BSR zone and presented herein allow for a pragmatic approach to consider the initiation of pyritization to maintain three-dimensionality, but timing, processes, and interrelationship of pyritization and instead experiences closure of the pyritization process before kerogenization. First, the pyritization process is likely initiated complete infilling of the Conotubus tube with pyrite. As such, in the BSR zone in the sediment column. The sediment column temporal limitation of one or more of the required chemical typically consists of an aerobic respiration zone just beneath the components, such as diffusive extinction of sulfate, may limit the water–sediment interface, followed by an anaerobic zone with extent of the BSR zone. With or without BSR zone restriction, nitrate, manganese and iron reduction, then the BSR zone, and the decaying Conotubus organism is likely pushed down into the finally the methanogenesis zone at depth (Fig. 7). For fossil methanogenesis zone due to high post-burial sedimentation rate, pyritization to occur in the BSR zone, factors directly responsible such that pyritization in the BSR zone is prematurely terminated. for BSR-mediated pyrite mineralization—the availability of Alternatively, these incompletely pyritized tubes may persist sulfate, reactive iron, metabolizable organic material and within the BSR zone, but with cessation of pyritization due to positioning of the carcass within the BSR zone—must overlap exhaustion of metabolizable organic material and a shortage of with commonly invoked facilitating conditions such as rapid exogenous carbon input. The interior space originally occupied by sedimentation and burial, low bioturbation and sediment anoxia. the Conotubus animal then becomes a central void, which is These factors are intimately related. For example, sedimentation subsequently infilled with carbonate cements. The timing of rate influences the availability of reactive iron, sulfate and organic carbonate cementation may depend on the electron donor used in carbon in the sediments, thus controlling the thickness of the BSR BSR (Supplementary Table 3). Two scenarios are plausible: zone and ultimately how much time the decaying carcass spends (1) the BSR respiration pathway does not produce acidity and here. Because sedimentation rate plays such an important role, we carbonate cementation is synchronous with pyritization; or propose a unifying model in which sedimentation rate was the (2) carbonate cementation follows dissipation of a lower pH primary factor controlling the pyritization–kerogenization microenvironment generated with BSR production of acidity. In gradient as observed in the Gaojiashan biota (Fig. 7). either case, no organic material remains or at least none is To help explain the model, we focus on four representative preserved through kerogenization. Regardless of which alternative preservational styles along the pyritization–kerogenization is more realistic, the true preservational distinction between gradient: (1) pervasive pyritization, (2) incomplete three- complete and incomplete three-dimensional pyritization hinges dimensional pyritization, (3) partial kerogenization with abun- on the duration, not the initiation, of pyrite formation. With dant pyrite association and (4) kerogenization with limited or regard to complete pyritization, we suggest that continuing pyrite highly diffuse pyrite association. For complete pyritization overgrowth is necessary for complete Conotubus tube infill, (Fig. 7a), initial pyrite mineralization must occur rapidly to whereas incompletely pyritized tubes instead are infilled with circumvent compression, and must continue to fill the entire carbonate cements after premature termination of pyritization. volume of the organism. If full pyritization occurs entirely in the At the other end of the Gaojiashan preservational spectrum are BSR zone, then the decaying carcass must stay in the BSR zone kerogenized carbonaceous compressions. While models for for a sufficient amount of time, requiring a thick BSR zone and/or kerogenization invoke the same facilitating taphonomic condi- a slow sedimentation rate following burial. The initial smothering tions for pyritization, three-dimensional structural rigidity is not event that entrapped the Conotubus organism rapidly placed it preserved, and instead organic tissues are stabilized to form below the oxic zone of aggressive aerobic decay, and subsequent geologically robust but two-dimensionally compressed carbonac- sedimentation proceeded sufficiently slowly to ensure a long eous remains. In the kerogenization taphonomic modes, enough duration in the BSR zone for complete pyritization. This pyritization is necessarily limited for tissues to be preserved as scenario is consistent with the d S data, with greater outer- carbonaceous compressions. The potential key is a rapid post- PY edge values suggesting an initial period of relatively rapid BSR, burial sedimentation rate and/or a narrower BSR zone, such that ensuring three-dimensional structural integrity, followed by a the fossilizing Conotubus tube is much more quickly moved progressive decrease in BSR rate (Supplementary Fig. 1) accom- through the BSR zone with little pyritization, thus positioning the panying greater isotopic fractionation and lower d S values. decaying organism within the methanogenesis zone shortly PY Volumetric considerations, however, suggest a shortage of following the onset of decay. In such a case, Conotubus tubes organic fuel from the Conotubus soft-tissue itself, which would that exhibit an appreciable amount of pyritization (Fig. 7c) may require either an exogenous source of carbon or production of have stayed in the BSR zone long enough to facilitate localized de novo organic carbon within the organic nucleus (for instance, pyritization but not extensively sustained for pyritization to by in situ chemoautotrophs) to continue fuelling further sulfide maintain three-dimensional structural integrity. Kerogenized production once the labile soft tissues of Conotubus were Conotubus with only diffuse pyrite (Fig. 7d) likely experience exhausted. Alternatively, pyritization could continue in the the majority of preservation within the methanogenesis zone methanogenesis zone where BSR is disfavoured but residual or during the earliest stages of decay, thus spending only very – 47 downward-diffusing porewater HS (or Fe–S complexes ) limited time in the BSR zone due to a high post-burial support pyrite overgrowth and continued pyritization. This sedimentation rate and/or a narrowed BSR zone. Following extended period of overgrowth may not show any clear textural these conditions, the fossil is predominantly comprised of change, but would obscure the anticipated U-shaped d S carbonaceous remains from kerogenization within the PY NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 9 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 methanogenesis zone. Methanogens are incapable of decompos- northwest margin of the Yangtze Platform (Supplementary Fig. 2A), the Gaojiashan region has numerous exposures of Ediacaran–Cambrian strata with ing higher molecular weight organic compounds, commonly broadly similar stratigraphy (from lower to upper): siliciclastic-dominated using acetate as the terminal electron acceptor (generalized: Doushantuo Formation; dolostone-dominated Dengying Formation; and – – CH COO þ H O-CH þ HCO ). If the breakdown of high- 3 2 4 3 phosphorite and carbonate of the basal Cambrian Kuanchuanpu Formation. molecular weight compounds via bacterial fermentation The Dengying Formation is tripartite (Supplementary Fig. 2B), consisting of – – (from lower to upper): thick-bedded, vuggy, peritidal dolostones of the (generalized: C H O þ4H O-2CH COO þ 2 HCO þ 4 6 12 6 2 3 3 þ B300-m-thick Algal Dolomite Member; thin-bedded calcareous siltstones, H þ4H ) is mostly limited to metabolically labile tissues, and mudstones and limestones of the B55-m-thick Gaojiashan Member that hosts aggressive aerobic degradation (generalized: CH COO þ O -2 3 2 the Gaojiashan Lagersta¨tte; and thick-bedded, vuggy, microbially laminated-to- – 48 CO þ H O þ OH ) was limited as a result of rapid burial, only stromatolitic, peritidal dolostone of the B200-m-thick Beiwan Member. 2 2 Correlation with the radiometrically dated Dengying Formation in the Yangtze the most recalcitrant structures such as the Conotubus tube walls Gorges suggests that the Gaojiashan Lagersta¨tte is constrained between 551 and will enter the fossil record. A few alternative scenarios should also 51,52 541 Myr ago . be considered. First, the Conotubus remains may indeed undergo Gaojiashan fossils mostly occur within millimetric beds of fine-grained degradation within the BSR zone, but instead occupy calcisiltite-siltstone of the Gaojiashan Member, interpreted to have been deposited microenvironments that are substantially limited in either or below storm wave base. Biostratinomic analysis of the Gaojiashan biota indicates that rapid event deposition played a key role in the exceptional preservation of both reactive iron or sulfate thus hindering pyrite precipitation. Gaojiashan fossils . The Gaojiashan biota is dominated by weakly biomineralized Second, the invocation of minimal ambient organic material for to non-biomineralized tubular and ribbon-like fossils (for example, Cloudina, pyritization may not hold in cases of kerogenization. That is, SRB Conotubus, Gaojiashania, Shaanxilithes and Sinotubulites), and also includes may prefer disseminated organic sources if Conotubus is protolagenid microfossils, algal debris, ichnofossils and microbial mat 11,28,53–59 textures . The focus of this study, Conotubus hemiannulatus, is currently emplaced within comparatively more organic-rich sediments, only known from the Gaojiashan Lagersta¨tte. Showing similarities in construction with Conotubus thus avoiding BSR-degradation and localized (Fig. 1d) and epibenthic life-mode, Conotubus has been interpreted as a possible 28,55 pyritization. Regardless, in either case, organic degradation is evolutionary precursor of Cloudina . Conotubus differs from Cloudina in its clearly limited to labile tissues, such that only the recalcitrant tube composition, as Conotubus was likely only weakly biomineralized at most . The fossiliferous unit occurs B18–49 m above the base of the Gaojiashan Member, tissues are eventually preserved as kerogens. with the Conotubus–dominated biofacies within the 26–39 m range corresponding Previous biostratinomical analysis of the late Ediacaran 13 18 60 to positive d C and negative d O excursions . Rare earth elemental Gaojiashan Lagersta¨tte has established that event deposits played geochemistry suggests that the Gaojiashan Member was deposited in a restricted an important role in the preservation of Gaojiashan fossils , but shallow sea environment, with riverine influx, common storm deposition influence , and high bioproductivity. the post-burial mineralization processes leading to the observed The samples studied herein were collected from calcareous siltstones 28–45 m pyritization–kerogenization gradient of preservation remain above the base of the Gaojiashan Member (Supplementary Fig. 2B). Three pyritized elusive. On the basis of geochemical analyses of three- Conotubus hemiannulatus specimens, collected 28–29 m above the base of the dimensionally pyritized Conotubus specimens, we have Gaojiashan Member (%1 in Supplementary Fig. 2B), were trimmed to sub-25-mm established that the pyritization process proceeded centripetally pieces, vacuum embedded in low-viscosity epoxy, and then ground and polished to make two longitudinal cross-sections and one transverse cross-section. These three from a rim of micrometric pyrite nucleated on the tube wall and specimens (reposited at the University of Missouri, Columbia; specimen numbers: fuelled by SRB degradation of labile tissues within the tube. This GJS-Cono001 to GJS-Cono003) were imaged and compositionally analysed using process can be described using a diffusion–precipitation scanning electron microscopy (SEM)/energy-dispersive X-ray spectroscopy (EDS). 31,32 34 model , modified to account for the role of an organic tube Sulfur isotopic compositions of pyrite (d S , reported as %-VCDT) were PY measured in situ using SIMS and on microdrilled powders using IRMS. A fourth in promoting the onset of pyritization by providing a preferable specimen, collected at 37–38 m above the base of the Gaojiashan Member (%3in substrate for nucleation. We suggest that preservation along the Supplementary Fig. 2B), on a larger slab was polished to make a transverse pyritization–kerogenization gradient can be understood as cross-section. This specimen (reposited at the Virginia Tech; specimen number: variations in the placement and duration of the carcass within 1GH2-70A) was analysed using SEM/EDS, ultraviolet photoluminescence microscopy and in situ X-ray diffraction (XRD). Both specimen number 1GH-70A the BSR and methanogenesis zones. The amount of time spent in and a non-fossiliferous slab, collected at 44–45 m above the base of the Gaojiashan each zone is principally influenced by post-burial sedimentation Member (%4 in Supplementary Fig. 2B), were microdrilled for IRMS d C and rate and/or BSR zone thickness, the latter of which is also related d O analyses (see Fig. 6a,b for drilling maps). An additional slab, collected 32 m to the availability of metabolizable organic material and sulfate. above the base of the Gaojiashan Member (%2 in Supplementary Fig. 2B), was analysed via IRMS for d S (data reported in Supplementary Table 1). The fossils that show three-dimensional pyritization, whether CAS pervasive or incomplete, spend more time in the BSR zone. In contrast, those that are two-dimensional carbonaceous Scanning electron microscopy. All SEM and EDS analyses (Fig. 2a–c,g; and Fig, 3a,c; Fig. 4a,b,e–g; Fig. 5b,e,f) were conducted using an FEI company Quanta compressions, either with extensive or diffuse pyrite association, 600 field-emission variable-pressure SEM with an integrated Bruker AXS Quantax are more rapidly buried in the methanogenesis zone. In each case, 400 high-speed silicon-drift EDS detector (Virginia Tech Institute for Critical degradation is required for preservation, and each mode may be Technology and Applied Science Nanoscale Characterization and Fabrication viewed as a complex balance between decay and mineralization. Laboratory). The specimens were analysed in high-vacuum mode (B6  10 Torr), B10 mm working distance, 20 keV beam accelerating voltage, 5.0 spot size These preservation processes, whether pyritization or (approximation of beam diameter and specimen current) and a system take-off kerogenization, are governed by the same suite of facilitating angle of 35 for EDS analyses. EDS point scans were conducted for 100 s live-time, taphonomic conditions, are primarily influenced by microbial and elemental maps were collected for 600 s live-time. decay pathways, and differ principally in the duration of interactions with the BSR and methanogenesis zones. Thus, the Secondary ion mass spectroscopy. All SIMS analyses followed d S methods PY scientific conversation regarding contributing factors of Beecher’s described in ref. 32, using a Cameca 7f GEO magnetic sector system (Virginia Tech Trilobite-type pyritization and Burgess Shale-type carbonaceous Institute for Critical Technology and Applied Science Nanoscale Characterization and Fabrication Laboratory). A Cs primary beam with 1 nA current at an energy compression should be shifted from facilitating factors such as a 32 34 49,50 18 of 20 kV was used to sputter the specimen, and the S and S isotopes were lack of bioturbation and bed-capping carbonate cements ,to detected using dual Faraday cup detectors from a B10 mm analytical spot. Mass those that drive mineralization and stabilization processes and are 32 16 resolution of B2,000 m per Dm was used to resolve the S from O mass directly responsible for fossil preservation. interference. A total of 214 spots across three specimens were analysed (Supplementary Table 1; Figs 2a,d–f; Fig. 3a,b; Fig. 4b–d), and measured d S PY values are reported as % deviation from VCDT (Vienna Canon Diablo Troilite; 34 32 Methods S/ S ¼ 0.0450045 ref. 61) calibrated via a Balmat pyrite standard 34 34 32 Materials. The Conotubus hemiannulatus specimens examined in this study were (d S ¼ 15.1%-VCDT; S/ S ¼ 0.04568407 refs 62,63). Each SIMS spot Balmat 34 32 collected from the Gaojiashan Member of the Dengying Formation at Gaojiashan measurement consisted of 10 cycles of S/ S ratios acquired from the same in Ningqiang county, southern Shaanxi Province, South China . Located in the physical spot after B2-min presputter to remove potential surface contamination. 10 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved. NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 ARTICLE The duration of individual spot analyses was B5 min, not including presputter. ´ 13. Farrell, U. C., Briggs, D. E. G., Hammarlund, E. H., Sperling, E. A. & Gaines, R. One-sigma errors of sample d S measurements were calculated from the PY R. Paleoredox and pyritization of soft-bodied fossils in the Ordovician instrumental standard error report of the 10 cycles, converted to %-VCDT. Frankfort Shale of New York. Am. J. Sci. 313, 452–489 (2013). 14. Raiswell, R. et al. Turbidite depositional influences on the diagenesis of Beecher’s Trilobite Bed and the Hunsruck Slate; sites of soft tissue pyritization. Ultraviolet photoluminescence and X-ray diffraction. Photoluminescence Am. J. Sci. 308, 105–129 (2008). microscopy and in situ XRD analyses were conducted on a UV microscope 15. Gaines, R. R. et al. Burgess shale  type biotas were not entirely burrowed away. (Olympus BX51) and a Rigaku Rapid II X-ray diffraction system with a 2D image Geology 40, 283–286 (2012). plate, in the S.W. Bailey X-ray Diffraction Laboratory, Department of Geoscience, 16. Orr, P. J., Briggs, D. E. G. & Kearns, S. L. Cambrian Burgess Shale animals University of Wisconsin. The polished cross-sectional slab of Conotubus, specimen replicated in clay minerals. Science 281, 1173–1175 (1998). number 1GH2-70A, was used in the analyses. All diffraction patterns were col- 17. Petrovich, R. Mechanisms of fossilization of the soft-bodied and lightly lected using reflection mode. Single-crystal diffraction patterns were also obtained armored faunas of the Burgess Shale and of some other classical localities. Am. to understand the crystallographic relationship between the dolomite and calcite in J. Sci. 301, 683–726 (2001). the zoned crystals (Fig. 5c,d,g). 18. Gaines, R. R. et al. Mechanism for Burgess Shale-type preservation. Proc. Natl Acad. Sci. USA 109, 5180–5184 (2012). 19. Butterfield, N. J. Does cement-induced sulfate limitation account for Burgess Isotope ratio mass spectroscopy. Carbon and oxygen IRMS analyses were Shale-type preservation? Proc. Natl Acad. Sci. USA 109, E1901 (2012). carried out at the University of Maryland and the Northwest University in Xi’an. 20. Xiao, S., Yuan, X., Steiner, M. & Knoll, A. H. Macroscopic carbonaceous Approximately 100 mg microdrilled powder was allowed to react for 10 min at compressions in a terminal Proterozoic shale: a systematic reassessment of the 90 C with anhydrous H PO in a Multiprep inlet system connected to an 3 4 Miaohe biota, South China. J. Paleontol. 76, 345–374 (2002). 13 18 Elementar Isoprime dual inlet mass spectrometer for d C and d O analysis. 21. Anderson, E. P., Schiffbauer, J. D. & Xiao, S. Taphonomic study of organic- Isotopic results are expressed in the standard d notation as % deviation from walled microfossils confirms the importance of clay minerals and pyrite in VPDB. Uncertainties determined by multiple measurements of NBS-19 were better Burgess Shale-type preservation. Geology 39, 643–646 (2011). than 0.05% (1s) for both C and O isotopes. 22. Gaines, R. R., Briggs, D. E. G. & Yuanlong, Z. Cambrian Burgess Shale–type Carbonate-associated sulfate sulfur IRMS analysis was carried out at Indiana deposits share a common mode of fossilization. Geology 36, 755–758 (2008). University. After trimming to remove visible veins and weathering rinds and 23. Van Roy, P. et al. Ordovician faunas of Burgess Shale type. Nature 465, ultrasonically cleaning in distilled deionized water, 56.3 g of whole rock was 215–218 (2010). crushed and pulverized into powder of o200 mesh size (74 mm) using a split- 24. Lin, J.-P. & Briggs, D. E. G. Burgess Shale-type preservation: a comparison of discus mill. Sulfate extraction followed the recommended protocol of ref. 64. Ultra- Naraoiids (Arthropoda) from three Cambrian localities. Palaios 25, 463–467 pure Milli-Q water (18 MO), purified NaCl, and distilled HCl were used to create (2010). solutions for leaching and acid digestion of the sample. The powder was immersed 25. Fike, D. A. & Grotzinger, J. P. A paired sulfate–pyrite d S approach to in 10% NaCl solution under constant magnetic stirring at room temperature until understanding the evolution of the Ediacaran–Cambrian sulfur cycle. Geochim. no sulfate was present in filtrate solutions. After water-leaching steps, the carbonate Cosmochim. Acta 72, 2636–2648 (2008). sample was dissolved in 10% HCl solution. The slurry was decanted and vacuum 26. Lin, S., Zhang, Y., Zhang, L., Tao, X. & Wang, M. Body and trace fossils of filtered through a 0.45-mm cellulose membrane filter. The acid-leached sulfate was metazoa and algal macrofossils from the upper Sinian Gaojiashan Formation in collected as BaSO by adding saturated BaCl solution. All collected BaSO samples 4 2 4 southern Shaanxi. Geol. Shaanxi 4, 9–17 (1986). were further purified by the DDARP method of ref. 65. BaSO was converted to SO using an Elemental Analyzer at 990 C and the d S measurement was 27. Farrell, U. C., Martin, M. J., Hagadorn, J. W., Whiteley, T. & Briggs, D. E. G. 2 CAS conducted on a Thermo-Electron Delta V Advantage mass spectrometer in Beyond Beecher’s Trilobite Bed: widespread pyritization of soft tissues in the continuous-flow mode. Late Ordovician Taconic foreland basin. Geology 37, 907–910 (2009). In addition, pyrite from samples GJS-Cono001 to GJS-Cono003 was 28. Cai, Y., Schiffbauer, J. D., Hua, H. & Xiao, S. Morphology and paleoecology of microdrilled and analysed for d S (s.d. ¼ 0.3%) to compare with SIMS PY the late Ediacaran tubular fossil Conotubus hemiannulatus from the Gaojiashan results. Pyrite extraction followed the chromium reduction method of ref. 66. Lagersta¨tte of southern Shaanxi Province, South China. Precambrian Res. 191, Sulfur isotopic results are expressed in the standard d notation as % deviation 46–57 (2011). from VCDT. 29. Bartels, C., Briggs, D. E. G. & Brassel, G. The Fossils of the Hunsru¨ck Slate: Marine Life in the Devonian 309 (Cambridge Univ. Press, 1998). 30. Bergstro¨m, J., Briggs, D. E. G., Dahl, E., Rolfe, W. D. I. & Stu¨rmer, W. Nahecaris References stuertzi, a phyllocarid crustacean from the Lower Devonian Hunsru¨ck Slate. 1. Cai, Y., Schiffbauer, J. D., Hua, H. & Xiao, S. Preservational modes in the Pala¨ontologische Zeitschrift 61, 273–298 (1987). Ediacaran Gaojiashan Lagersta¨tte: pyritization, aluminosilicification, and 31. Raiswell, R., Whaler, K., Dean, S., Coleman, M. L. & Briggs, D. E. G. A simple carbonaceous compression. Palaeogeogr. Palaeoclimatol. Palaeoecol. 326-328, three-dimensional model of diffusion-with-precipitation applied to localised pyrite formation in framboids, fossils and detrital iron minerals. Mar. Geol. 109–117 (2012). 2. Briggs, D. E. G. The role of decay and mineralization in the preservation of soft- 113, 89–100 (1993). bodied fossils. Annu. Rev. Earth Planet. Sci. 31, 275–301 (2003). 32. Xiao, S., Schiffbauer, J. D., McFadden, K. A. & Hunter, J. Petrographic and 3. Seilacher, A. Begriff and bedeutung der Fossil-Lagersta¨tten. N. Jb. Geol. SIMS pyrite sulfur isotope analyses of Ediacaran chert nodules: implications for Palaontol. Abh. 1970, 34–39 (1970). microbial processes in pyrite rim formation, silicification, and exceptional fossil 4. Allison, P. A. & Briggs, D. E. G. Exceptional fossils record: distribution of soft- preservation. Earth Planet. Sci. Lett. 297, 481–495 (2010). tissue preservation through the Phanerozoic. Geology 21, 527–530 (1993). 33. Berner, R. A. Sedimentary pyrite formation: an update. Geochim. Cosmochim. 5. Schiffbauer, J. D. & Laflamme, M. Lagersta¨tten through time: a collection of Acta 48, 605–615 (1984). exceptional preservational pathways from the terminal Proterozoic through 34. Wallace, A. F., De Yoreo, J. J. & Dove, P. M. Kinetics of silica nucleation on today. Palaios 27, 275–278 (2012). carboxyl- and amine-terminated surfaces: insights for biomineralization. J. Am. 6. Butterfield, N. J. Exceptional fossil preservation and the Cambrian Explosion. Chem. Soc. 131, 5244–5250 (2009). Integr. Comp. Biol. 43, 166–177 (2003). 35. Giuffre, A. J., Hamm, L. M., Han, N., De Yoreo, J. J. & Dove, P. M. 7. Xiao, S. & Schiffbauer, J. D. in From Fossils to Astrobiology: Cellular Origin, Life Polysaccharide chemistry regulates kinetics of calcite nucleation through in Extreme Habitats and Astrobiology (eds Seckbach, J. & Walsh, M.) 89–118 competition of interfacial energies. Proc. Natl Acad. Sci. USA 110, 9261–9266 (Springer, 2009). (2013). 8. Canfield, D. E. & Raiswell, R. in Taphonomy; releasing the data locked in the 36. Wood, T. L. & Garrels, R. M. Thermodynamic Values at Low Temperature for fossil record (eds Allison, Peter A. & Briggs, Derek E. G.) 337–387 (Plenum Natural Inorganic Materials (Oxford Univ. Press, 1987). Press, 1991). 37. Boudreau, B. P. & Canfield, D. E. A provisional diagenetic model for pH in 9. Briggs, D. E. G., Raiswell, R., Bottrell, S. H., Hatfield, D. & Bartels, C. Controls anoxic porewaters. J. Mar. Res. 46, 429–455 (1988). on the pyritization of exceptionally preserved fossils: an analysis of the Lower 38. Middelburg, J. J. A simple rate model for organic matter decomposition in Devonian Hunsrueck Slate of Germany. Am. J. Sci. 296, 633–663 (1996). marine sediments. Geochim. Cosmochim. Acta 53, 3581–3595 (1989). 10. Cai, Y. & Hua, H. Pyritization in the Gaojiashan Biota. Chinese Sci. Bull. 52, 39. Canfield, D. E. & Raiswell, R. in Taphonomy: Releasing the Data Locked in 645–650 (2007). the Fossil Record, Volume 9 of Topics in Geobiology (eds Allison, P. A. & 11. Cai, Y., Hua, H., Xiao, S., Schiffbauer, J. D. & Li, P. Biostratinomy of the late Briggs, D. E. G.) 411–453 (Plenum Press, 1991). Ediacaran pyritized Gaojiashan Lagersta¨tte from southern Shaanxi, South 40. Zhang, F., Yan, C., Teng, H., Roden, E. E. & Xu, H. In situ AFM observations of China: importance of event deposits. Palaios 25, 487–506 (2010). Ca-Mg carbonate crystallization catalyzed by dissolved sulfide: Implications for 12. Gabbott, S. E., Hou, X. G., Norry, M. J. & Siveter, D. J. Preservation of Early sedimentary dolomite formation. Geochim. Cosmochim. Acta 105, 44–55 Cambrian animals of the Chengjiang biota. Geology 32, 901–904 (2004). (2013). NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications 11 & 2014 Macmillan Publishers Limited. All rights reserved. ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms6754 41. Braissant, O. et al. Exopolymeric substances of sulfate-reducing bacteria: 62. Crowe, D. E. & Vaughan, R. G. Characterization and use of isotopically 34 32 Interactions with calcium at alkaline pH and implication for formation of homogeneous standards for in situ laser microprobe analysis of S/ S ratios. carbonate minerals. Geobiology 5, 401–411 (2007). Am. Mineral. 81, 187–193 (1996). 42. Habicht, K. S. & Canfield, D. E. Isotope fractionation by sulfatereducing natural 63. Kohn, M. J., Riciputi, L. R., Stakes, D. & Orange, D. L. Sulfur isotope variability populations and the isotopic composition of sulfide in marine sediments. in biogenic pyrites: reflections of heterogeneous bacterial colonization? Am. Geology 29, 555–558 (2001). Mineral. 83, 1454–1468 (1998). 43. Li, C. et al. A stratified redox model for the Ediacaran ocean. Science 328, 80–83 64. Wotte, T., Shields-Zhou, G. A. & Strauss, H. Carbonate-associated sulfate: (2010). experimental comparisons of common extraction methods and 44. Raiswell, R. & Berner, R. A. Pyrite and organic matter in Phanerozoic normal recommendations toward a standard analytical protocol. Chem. Geol. 326, marine shales. Geochim. Cosmochim. Acta 50, 1967–1976 (1986). 132–144 (2012). 45. Canfield, D. E., Raiswell, R. & Bottrell, S. H. The reactivity of sedimentary iron 65. Bao, H. Purifying barite for oxygen isotope measurement by dissolution and minerals toward sulfide. Am. J. Sci. 292, 659–683 (1992). reprecipitation in a chelating solution. Anal. Chem. 78, 304–309 (2006). 46. Berner, R. A. A new geochemical classification of sedimentary environments. 66. Canfield, D. E., Raiswell, R., Westrich, J. T., Reaves, C. M. & Berner, R. A. J. Sediment. Petrol. 51, 359–365 (1981). The use of chromium reduction in the analysis of reduced inorganic sulfur in 47. Rickard, D. & Luther, III G. W. Chemistry of iron sulfides. Chem. Rev. 107, sediments and shale. Chem. Geol. 54, 149–155 (1986). 514–562 (2007). 67. Froelich, P. N. Early oxidation of organic matter in pelagic sediments of the 48. Konhauser, K. O. Introduction to Geomicrobiology (Blackwell Publishing, 2007). eastern equitorial Atlantic: Suboxic diagenesis. Geochim. Cosmochim. Acta 43, 49. Allison, P. A. & Briggs, D. E. G. Burgess Shale biotas; burrowed away? Lethaia 1075–1090 (1979). 26, 184–185 (1993). 50. Orr, P. J., Benton, M. J. & Briggs, D. E. G. Post-Cambrian closure of the deep-water slope-basin taphonomic window. Geology 31, 769–772 (2003). Acknowledgements 51. Condon, D. et al. U-Pb ages from the Neoproterozoic Doushantuo Formation, This research was supported by funding through NASA Exobiology and Evolutionary China. Science 308, 95–98 (2005). Biology Program, NASA Astrobiology Institute (N07-5489), National Science Founda- 52. Bowring, S. A. et al. Geochronologic constraints on the chronostratgraphic tion (EAR-0824890, EAR095800, EAR1124062), Chinese Academy of Sciences, National framework of the Neoproterozoic Huqf Supergroup, Sultanate of Oman. Am. J. Natural Science Foundation of China (41202006; 41030209; 41272011), Chinese Ministry Sci. 307, 1097–1145 (2007). of Science and Technology, Virginia Tech Institute for Critical Technology and Applied 53. Cai, Y., Hua, H., Schiffbauer, J. D., Sun, B. & Xiao, S. Tube growth patterns and Sciences and China Postdoctoral Science Foundation (2013M531410). We would like to microbial mat-related lifestyles in the Ediacaran fossil Cloudina, Gaojiashan thank K.L. Shelton and J.W. Huntley for insightful discussion. Lagersta¨tte, South China. Gondwana Res. 25, 1008–1018 (2014). 54. Chen, Z., Bengtson, S., Zhou, C., Hua, H. & Yue, Z. Tube structure and original composition of Sinotubulites: Shelly fossils from the late Neoproterozoic in Author contributions southern Shaanxi, China. Lethaia 41, 37–45 (2008). J.D.S. designed the research with input from S.X. and Y.C. S.X. supervised the research. 55. Hua, H., Chen, Z. & Yuan, X. The advent of mineralized skeletons in J.D.S, S.X., Y.C. and H.H. performed the fieldwork. Sample preparation was performed Neoproterozoic Metazoa: new fossil evidence from the Gaojiashan Fauna. Geol. by J.D.S. and Y.C., SEM and EDS analysis was performed by J.D.S., SIMS analysis was J. 42, 263–279 (2007). performed by J.D.S. and J.H., ultraviolet and XRD analysis was performed by H.X., IRMS 56. Hua, H., Chen, Z., Yuan, X., Xiao, S. & Cai, Y. The earliest Foraminifera from analysis performed by Y.C., Y.P. and A.J.K. and geochemical data analysis was performed southern Shaanxi, China. Sci. China D 53, 1756–1764 (2010). by J.D.S., S.X. and A.F.W. J.D.S., with significant input from all of the authors, wrote the 57. Hua, H., Chen, Z., Yuan, X., Zhang, L. & Xiao, S. Skeletogenesis and asexual paper. reproduction in the earliest biomineralizing animal Cloudina. Geology 33, 277–280 (2005). Additional information 58. Hua, H., Pratt, B. R. & Zhang, L. Borings in Cloudina shells: complex predator- prey dynamics in the terminal Neoproterozoic. Palaios 18, 454–459 (2003). Supplementary Information accompanies this paper at http://www.nature.com/ 59. Meyer, M., Schiffbauer, J. D., Xiao, S., Cai, Y. & Hua, H. Taphonomy of the late naturecommunications Ediacaran enigmatic ribbon-like fossil Shaanxilithes. Palaios 27, 354–372 Competing financial interests: The authors declare no competing financial interests. (2012). 60. Zhang, P., Hua, H. & Liu, W. Isotopic and REE evidence for the Reprints and permission information is available online at http://npg.nature.com/ paleoenvironmental evolution of the late Ediacaran Dengying Section, reprintsandpermissions/ Ningqiang of Shaanxi Province, China. Precambrian. Res. 242, 96–111 (2014). 61. Ault, W. V. & Jensen, M. L. in Biogeochemistry of Sulfur Isotopes: National How to cite this article: Schiffbauer, J. D. et al. A unifying model for Neoproterozoic– Science Foundation Symposium Proceedings. (ed. Jensen, M. L.) 16–29 Palaeozoic exceptional fossil preservation through pyritization and carbonaceous (Yale Univ. Press, 1962). compression. Nat. Commun. 5:5754 doi: 10.1038/ncomms6754 (2014). 12 NATURE COMMUNICATIONS | 5:5754 | DOI: 10.1038/ncomms6754 | www.nature.com/naturecommunications & 2014 Macmillan Publishers Limited. All rights reserved.

Journal

Nature CommunicationsSpringer Journals

Published: Dec 17, 2014

There are no references for this article.