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The geobiological nitrogen cycle: From microbes to the mantle

The geobiological nitrogen cycle: From microbes to the mantle Centre for Exoplanet Science, University of St Andrews, St Andrews, Fife, UK Nitrogen forms an integral part of the main building blocks of life, including DNA, RNA, and proteins. N is the dominant gas in Earth’s atmosphere, and nitrogen is stored in Correspondence 2 A. L. Zerkle, School of Earth & Environmental all of Earth’s geological reservoirs, including the crust, the mantle, and the core. As Sciences and Centre for Exoplanet Science, such, nitrogen geochemistry is fundamental to the evolution of planet Earth and the University of St Andrews, St Andrews, Fife, UK. life it supports. Despite the importance of nitrogen in the Earth system, large gaps Email: az29@st-andrews.ac.uk remain in our knowledge of how the surface and deep nitrogen cycles have evolved Funding information over geologic time. Here, we discuss the current understanding (or lack thereof) for Natural Environmental Research Council how the unique interaction of biological innovation, geodynamics, and mantle petrol- Fellowship, Grant/Award Number: NE/ H016805 ogy has acted to regulate Earth’s nitrogen cycle over geologic timescales. In particular, we explore how temporal variations in the external (biosphere and atmosphere) and internal (crust and mantle) nitrogen cycles could have regulated atmospheric pN . We consider three potential scenarios for the evolution of the geobiological nitrogen cycle over Earth’s history: two in which atmospheric pN has changed unidirectionally (in- creased or decreased) over geologic time and one in which pN could have taken a dramatic deflection following the Great Oxidation Event. It is impossible to discrimi- nate between these scenarios with the currently available models and datasets. However, we are optimistic that this problem can be solved, following a sustained, open- minded, and multidisciplinary effort between surface and deep Earth communities. 1  |  INTR ODUCTION The chemistry of Earth’s atmosphere is in a constant state of dis- equilibrium due to atmospheric photochemistry, life’s collective me- Understanding the nitrogen cycle is part of a dynamic geobiological tabolisms, chemical weathering, and the large- scale geochemical fluxes puzzle, for which the ultimate goal is illuminating the mechanics re- imposed by plate tectonics and related volcanism (Bebout, Fogel, & sponsible for the development of habitability on Earth and on other Cartigny, 2013). However, atmospheric chemistry is not a constant planets, in our solar system and beyond. For example, nitrogen is a key though time (Barry & Hilton, 2016; Mikhail & Sverjensky, 2014). The element in the structure of amino acids, proteins, nucleic acids, and most dramatic geochemical transition since the formation of the at- other molecules vital to life and is also the dominant component of mosphere was biological rather than geological in nature. Sometime in Earth’s atmosphere. In addition, the oxidation of ammonic nitrogen the mid- to late Archean (e.g., Farquhar, Zerkle, & Bekker, 2011), mi- (NH ) in the mantle has been proposed as a source of liquid water crobial life developed the ability to perform oxygenic photosynthesis, to the early Earth (Li & Keppler, 2014), and N could have played an which uses energy from the sun and raw materials extracted from the important role in maintaining Earth’s surface above the freezing point geosphere (CO + H O) to generate energy, construct essential building 2 2 of water in the presence of the faint young sun (e.g., Goldbla tt et al., materials, and releases oxygen in a gas phase (O ) as a waste product. 2009). Over time this biological revelation cumulatively oxygenated Earth’s This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2017 The Authors Geobiology Published by John Wiley & Sons Ltd Geobiology. 2017;15:343–352. wileyonlinelibrary.com/journal/gbi     343 Denitrification remin. Upwelling ZERKLE and MIKHaIL 344       surface. The result is that Earth’s atmosphere became highly reactive, NO to N ) and anaerobic ammonium oxidation (anammox, the oxi- 3 2 + − unlike the atmospheres of Mars and Venus which are still dominated by dation of NH to N using NO ; Dalsgaard, Thamdrup, & Canfield, 4 2 2 unreactive gases (CO + N ). The combination of a uniquely reactive- 2005). These processes, which result in the loss of fixed N from the 2 2 gas- rich atmosphere and hydrosphere, coupled with subduction zone biosphere, occur in soils, marine sediments, and oxygen minimum plate tectonics, means that Earth injects oxidizing material into a rel- zones, completing the biological nitrogen cycle (Figure 1). atively reduced mantle (Frost & Mccammon, 2008; Kelley & Cottrell, All life requires N in a reduced form, which can either be taken up 2009). This phenomenon is seemingly unique because such biological directly as ammonium or enzymatically reduced during nitrate assimi- and tectonic processes are only known to occur on Earth. Here, we lation. Once assimilated into biomass, organic nitrogen is recycled via compare and contrast current ideas for how this unique interaction of release and re- assimilation of organic N within the surface ocean, or biological innovation, geodynamics, and mantle petrology could have subsequently regenerated during organic maertt remineralization in acted to regulate the geobiological nitrogen cycle over Earth history. sediments. Over geologic timescales, some small amount of fixed nitro- gen can leak out of the biosphere–ocean system and be buried in the sediments, as organic nitrogen or as remineralized ammonium incorpo- 2  |  B A CK GR OUND rated into clays during diagenesis (Schroeder & McLain, 1998). During burial, nitrogen- bearing rocks can undergo metamorphism, which can 2.1 | Surficial nitrogen cycle return a significant fraction of the nitrogen back to the atmosphere Molecular nitrogen in the gas- phase (N ) is the largest surficial res- (e.g., Haendel, Mühle, Nitzsche, Stiehl, & Wand, 1986). The remainder ervoir of nitrogen and comprises around 78% of Earth’s atmosphere. of N entrained within sediments can be subducted, along with nitrogen Atmospheric nitrogen is incorporated into the biosphere via the pro- sequestered into altered oceanic lithosphere as ammonium and organic cess of N fixation, whereby specialized prokaryotes convert this inert species (Busigny, Cartigny, & Philippot, 2011; Halama, Bebout, John, & N gas into biomolecules (as C- NH ) (Figure 1). Nitrogen fixation is an Scambelluri, 2014). This subduction of sediment and altered oceanic 2 2 energetically expensive process which requires 16 ATP to break the lithosphere constitutes the primary flux of surficial N into the deep triply bonded N molecule. N - fixing organisms (termed “diazotrophs”) Earth. 2 2 accomplish this feat by utilizing the nitrogenase metallo- enzyme com- plex, which contains Fe and Mo in its most efficient form. 2.2 | Deep earth nitrogen cycle Nitrogen fixed as ammonium (NH ) is dominantly recycled by the − − biosphere or sequentially oxidized to nitrite (NO ) and nitrate (NO ). Once subducted into the deep Earth, nitrogen has historically been 2 3 Ammonium oxidation (“nitrification”) generally requires molecular considered an unreactive gas in the field of mantle geochemistry, oxygen (Carlucci & Mcnally, 1969). These “oxidized” nitrogen com- owing to the strength of the covalent triple N- bond, and abundance pounds provide an important nutrient source for eukaryotic primary of N in the atmosphere (e.g., Boyd & Pillinger, 1994; Javoy, Pineau, producers. Alternatively, nitrate (and some nitrite) can also be reduced & Delorme, 1986). Consequently, the behavior of nitrogen has tradi- back to ammonium via dissimilatory nitrate reduction to ammonium tionally been assumed to be akin to the unreactive noble gases (e.g., (DNRA), another process that was described fairly recently in the mod- Bergin, Blake, Ciesla, Hirschmann, & Li, 2015; Halliday, 2013; Marty, ern system (Lam et al., 2009). 1995, 2012; Mikhail, Dobosi, Verchovsky, Kurat, & Jones, 2013). Fixed nitrogen can be returned to the atmosphere as N via several However, empirical data show a diverse variety of nitrogen species chemotrophic metabolisms, including denitrification (the reduction of are present in the deep Earth, including molecular N , ammonium, FIGURE 1 Basin- scale model of the N N N N 2 2 2 2 modern marine biogeochemical nitrogen 2 N cycle. The red pathways are anaerobic Fixation Fixation pathways that would have presumably Norg + - + Norg NH NO NH dominated in anoxic Archean environments. 4 3 4 nit. recyc. The blue pathways require oxygen (or Uptake Burial an oxidized nitrogen species) and would presumably have proliferated after the Norg GOE. Note that for simplicity the nitrite - OMZ NH and nitrate pools are shown combined, 4 NO DNRA as NO . Additional abbreviations are as follows: OMZ = oxygen minimum zone NO3 (shown in purple); DNRA = dissimilatory nit. nitrate reduction to ammonium; nit. = NH nitrification; remin. = remineralization; Burial recyc. = recycling [Colour figure can be org viewed at wileyonlinelibrary.com] Anammox ZERKLE and MIKHaIL       345 we must rely on sparse data and predictive thermodynamic models to estimate past N dynamics. 3  |  DISCUSSION 3.1 | Evolution of the biogeochemical N cycle The emergence and evolution of biogeochemical nitrogen cycling over Earth history remains a major question mark in the field of geobiol- ogy (e.g., see recent review by Stüeken, Kipp, Koehler, & Buick, 2016). Abiotic N reduction to ammonium within hydrothermal systems could have supplied fixed nitrogen to an early deep biosphere (Brandes et al., 1998; Nishizawa, Miyazaki, Makabe, Koba, & Takai, 2014). Once an- oxygenic photosynthesis evolved sometime in the Archean, primary productivity would have been most abundant in the surface waters. FIGURE 2 The speciation of aqueous nitrogen at 5 GPa at Dry deposition or fixation by lightning could have provided an abi- 1000°C, calculated in equilibrium with Forsterite and Fayalite using otic supply of nitrogen to the surface oceans from the atmosphere the Deep Earth Water model (from Mikhail & Sverjensky, 2014) [Colour figure can be viewed at wileyonlinelibrary.com] (Navarro- Gonzalez, Mckay, & Mvondo, 2001). However, estimates of a very limited supply of nitrogen from these abiotic sources suggest that diamond (NC ), metallic nitride (Fe N, TiN, BN), and nitro- carbide (for N fixation must have evolved very early in life’s history to support an 3 3 2 comprehensive reviews of nitrogen in the deep Earth, see Bebout, ever- expanding biosphere (Haqq- Misra, Domagal- Goldman, Kasting, & Lazzeri, & Geiger, 2016; and Johnson & Goldblatt, 2015). All of the Kasting, 2008; Kasting & Siefert, 2001; Kharecha, Kasting, & Siefert, aforementioned species of nitrogen behave differently, where their 2005). Phylogenetic reconstructions of genes for the nitrogenase en- behavior can be described as compatible or incompatible to a host zyme support its early emergence (Boyd, Hamilton, & Peters, 2011; mineral phase, depending on charge and radius of the ion and the Fani, Gallo, & Lio, 2000; Raymond, Siefert, Staples, & Blankenship, occupation site in the mineral (Goldschmidt, 1924). For nitrogen in 2004; Weiss et al., 2016), possibly in an anoxic environment (Boyd & the mantle, recent experimentally and theoretically determined equi- Peters, 2013). In addition, the sedimentary δ N record suggests this librium constants have shown that ammonium should dominate over process could have been active as far back as ~3.2 Ga (Stüeken, Buick, molecular nitrogen in aqueous fluids in the uppermost mantle where Guy, & Koehler, 2015). Once N fixation was established, it is generally the redox state (fO ) is buffered below the quartz–fayalite–magnet- assumed that the input of nitrogen to the biosphere could keep pace ite buffer (QFM) (Li & Keppler, 2014; Mikhail & Sverjensky, 2014) with primary productivity as long as no other nutrient (e.g., phospho- (Figure 2). This is a significant insight, because for nitrogen, compat- rus or bioactive trace metals; Tyrrell, 1999; Anbar & Knoll, 2002) was ibility is directly related to speciation: Molecular nitrogen (N ) is limiting. highly incompatible, whereas ammonium (NH ) is likely compatible in As the speciation and microbial cycling of nitrogen are highly redox- potassium- bearing mineral phases (Watenphul, Wunder, & Heinrich, dependent, the biogeochemical nitrogen cycle would have changed 2009) and can dissolve as a trace component in potassium- absent significantly with the progressive oxygenation of Earth surface environ- phases (Li, Wiedenbeck, Shcheka, & Keppler, 2013; Watenphul, ments (e.g., Stüeken et al., 2016). Notably, in Earth’s Archean oceans Wunder, Wirth, & Heinrich, 2010). This is a crucial distinction from before the buildup of significant oxygen, processes involved in the the perspective of the global nitrogen cycle, because nitrogen in the modern N cycle that required molecular oxygen (or the presence of sig- molecular form is likely to be outgassed, while ammonium could be nificant quantities of oxidized N compounds) would have been absent. stored in mineral phases in the deep Earth (Mikhail & Sverjensky, In particular, nitrification, the stepwise oxidation of ammonium to ni- 2014). We explore this concept, and its potential response to changes trite and nitrate, requires at least some free oxygen (Carlucci & Mcnally, in global redox, in the discussion below. 1969). Thus, throughout the Archean and earliest Paleoproterozoic the Because Earth is a dynamic planet with active plate tectonics, nitrogen cycle would likely have consisted of N fixation followed by what goes into the mantle sometimes comes back out, and vice versa. burial and regeneration of NH in sediments (Figure 1). Therefore, the exchange of nitrogen between the surface and inte- Following widespread oxygenation of the marine biosphere during rior is governed by subduction (in- gassing) and volcanism (outgassing), the Great Oxidation Event (GOE) between ~2.4 and 2.3 Ga (e.g., re- and this interplay ultimately controls atmospheric N levels (Cartigny viewed in Farquhar, Zerkle, & Bekker, 2014), the primary N loss path- & Ader, 2003; Dauphas & Marty, 2004; Kerrich & Jia, 2004; Marty ways of denitrification and anammox proliferated to take advantage & Dauphas, 2003a,b). However, the further back one looks in time of the newly available oxidized N compounds (Zerkle et al., 2017). In the less data are available, and there is a predictable dearth of data the redox- stratified oceans that developed during this time period to constrain either the fluxes of nitrogen over geological time, or the (e.g., Poulton, Fralick, & Canfield, 2010; Scott et al., 2011; Zerkle et al., partial pressure of atmospheric nitrogen in the deep past. This means 2017), nitrification of ammonium- rich deep waters was confined to ZERKLE and MIKHaIL 346       the oxic–anoxic interface, with denitrification and anammox occurring a competitive advantage. Many researchers have suggested that N just below. fixation would also have been limited in the Proterozoic oceans, due The expansion of an aerobic N cycle during the GOE is supported to drawdown of bioactive trace metals required for nitrogenase (par- by temporal trends in sedimentary N isotope records, which show ticularly Mo) under widespread sulfidic conditions (Anbar & Knoll, a shift toward more positive δ N values similar to modern marine 2002). Metal limitation experiments with modern N - fixing cyano- values by ~2.3 Ga (Beaumont & Robert, 1999; Zerkle et al., 2017). bacteria suggest that vanishingly little Mo is actually required to sup- Studies of much older sediments (2.5–2.7 Ga) have interpreted tran- port modern rates of diazotrophy (down to ~5 nM; Zerkle, House, sitory increases in δ N as recording a temporary insurgence of oxi- Cox, & Canfield, 2006; Glass, Wolfe- Simon, & Anbar, 2009). Current dative N cycling, potentially related to localized transient increases in estimates of molybdenum concentrations in Precambrian oceans are marine O (Garvin, Buick, Anbar, Arnold, & Kaufman, 2009; Godfrey insufficient to resolve this issue at present (Reinhard, Raiswell, Scott, & Falkowski, 2009; Thomazo, Ader, & Philippot, 2011). These stud- Anbar, & Lyons, 2009; Scott et al., 2008). However, records of molyb- ies suggest that the aerobic N pathways could have evolved imme- denum in shales suggest that marine molybdenum levels rose to near diately following oxygenic photosynthesis, to take advantage of the modern levels at the end of the Neoproterozoic with enhanced oxida- newly available free oxygen in highly productive coastal environments. tive weathering during a second rise in atmospheric O (Sahoo et al., However, the isotope eect ff associated with these N loss pathways 2012), potentially further enhancing global N fixation rates. would only have been expressed once nitrite/nitrate was available at As the delivery of nitrogen to the sediments is intimately sufficient levels that their quantitative removal from the ocean did linked to the biosphere and dependent on redox and other en- not occur. Therefore, the shift toward more positive δ N values by vironmental parameters, the burial of nitrogen over geologic ~2.3 Ga (Zerkle et al., 2017) represents a turning point in the balance time (and thus its flux into the mantle) would have changed in − − of NO loss to NO supply, rather than the exact timing of when the response to these changes in the biogeochemical nitrogen cycle. 3 3 oxidative N cycle first evolved. Using conservative estimates for the timing of major biological The persistence of a deep anoxic water column after the emer- and geochemical innovations, we can propose a rough timeline gence of the aerobic N cycle could have had a dramatic eect ff on for changes in the burial of N into marine sediments over geologic the abundance of fixed nitrogen in the world’s oceans. Massive losses time (Figure 3). Nitrogen burial is thought to be generally driven of fixed nitrogen via denitrification and anammox are predicted to by changes in carbon burial over time (e.g., Berner, 2006), which have occurred during periods of deepwater anoxia (Canfield, Rosing, itself plays an important role in regulating Earth surface redox & Bjerrum, 2006; Fennel, Follows, & Falkowski, 2005), potentially conditions (e.g., Krissansen-Totton, Buick, & Catling, 2015). For limiting the availability of fixed inorganic nitrogen for primary produc- this calculation, we used the productivity estimates of Canfield, tion. These researchers suggest that such nitrogen limitation could Glazer and Falkowsk (2010) for primary production based on an have reduced the burial of organic carbon, and the resulting accumu- evolutionary progression of anoxygenic photoautotrophy, oxy- lation of atmospheric oxygen, eectiv ff ely hindering the evolution of genic photoautotrophy, and eukaryotic photoautotrophy. We uti- eukaryotes, as well as the continued oxygenation of Earth’s surface lized a constant burial rate of 10% total biomass (similar to the environments. Nitrogen isotope records from the Mesoproterozoic modern; Gruber, 2008) with a constant Redfield ratio of 6:1 (C:N). support nitrogen limitation, particularly within open ocean settings We used denitrification levels estimated from modern marine N (Stüeken, 2013). balances (e.g., Canfield et al., 2010; Gruber, 2008). The biggest The mid- Proterozoic nitrogen limitation hypothesis is predicated on unknown in this calculation is when coupled nitrification/denitri- the assumptions that the majority of primary productivity was occurring fication proliferated and how rates of denitrification responded via oxygenic photosynthesis in the surface ocean and that nitrogen fixa- to changes in ocean chemistry throughout the Proterozoic (as dis- tion could not keep pace with the fixed N loss (and the delivery of other cussed above). For this calculation, we assumed 25% of modern nutrients) to fuel this primary productivity. The evolution of oxygenic denitrification levels early in the GOE, and an increase to 130% photosynthesis in the late Archean would certainly have resulted in a associated with the subsequent buildup of a nitrate reservoir marked increase in global rates of primary production (Canfield et al., in a largely anoxic ocean, with large error bars to highlight this 2006). Johnston, Wolfe- Simon, Pearson, and Knoll (2009) point out uncertainty. Finally, we calculated changes in N fixation rates that anoxygenic photoautotrophs could also have made an important with enhanced molybdenum delivery during the Neoproterozoic contribution to primary productivity in the redox- stratified continen- Oxygenation Event (NOE) as a switch from molybdenum- limited tal margins that that seemingly dominated for much of the Proterozoic to modern N fixation rates, based on the experiments of Zerkle (e.g., Poulton et al., 2010; Sco tt et al., 2011). Primary producers in mar- et al. (2006). Note that this calculation does not consider any sig- ginal sulfidic zones could have had direct access to upwelling nutrients, nificant loss of nitrogen from the sediments during diagenesis or including ammonium, before it reached the redox interface and was lost metamorphic reactions prior to subduction. Notably, this scenario to nitrification–denitrification and anammox reactions. for changes in nitrogen burial over time predicts a progressive Consumption of upwelling ammonium by anoxygenic phototro- increase in the delivery of nitrogen to the deep Earth via sub- phs could have further contributed to the fixed nitrogen deficit in duction (with the exception of the possible mid- Proterozoic mini- surface waters, such that N - fixing organisms in the photic zone had mum) following an ever- increasingly efficient biosphere. 2 % Modern N burial ZERKLE and MIKHaIL       347 GOE NOE - - Low [NO ] High [NO ] Low [Mo] High [Mo] 3 3 Oxygenic photosynthesis Anoxygenic photosynthesis Origin of life Archean Proterozoic Phan. 4000 2500 542 0 Time (Ma) FIGURE 3 Estimated burial flux of nitrogen through time, following calculations described in the text [Colour figure can be viewed at wileyonlinelibrary.com] and Kr—elements that are far more akin to Xe in terms of geochemi- 3.2 | The missing nitrogen conundrum cal behavior, and in the case of Kr, mass. Another explanation is that Our understanding of the evolution of the deep Earth nitrogen cycle there exists a hidden nitrogen reservoir in the deep Earth, inferred to and the relevant nitrogen reservoirs is even less well constrained. be the core or unspecified deep mantle domain (Barry & Hilton, 2016; One puzzle often cited is the “missing nitrogen conundrum,” which Halliday, 2013; Marty, 2012). This reservoir is unlikely to be the core follows because the abundance of nitrogen in the bulk silicate Earth because carbon is more siderophile than nitrogen (Dalou, Hirschmann, (BSE) appears to be significantly lower than that of other volatile von der Handt, Mosenfelder, & Armstrong, 2016); therefore, a mantle elements (Figure 4). The most striking feature of these data is the reservoir is more in line with what is known about the partitioning of depletions shown for Xe and N, which could mean that these two el- carbon and nitrogen during core formation. Furthermore, stable iso- ements with contrasting behaviors and masses were both lost early tope data for diamonds show that nitrogen is subducted back into in Earth’s history (Bergin et al., 2015) without also depleting Ne, Ar, the deep mantle, implying nitrogen retention during subduction to at least the minimum depth of diamond stability (≥150 km; Mikhail et al., 2014) and possibly into the lower mantle (≥660 km; Palot, Cartigny, Harris, Kaminsky, & Stachel, 2012). This requires a mechanism to transport nitrogen beyond the mantle wedge. Note that Figure 4 is derived by summing up the assumed abun- dance of nitrogen in the BSE with the surficial reservoir; however, these values were calculated using N /Ar ratios, which is now known to be inaccurate for the majority of the mantle. In particu- lar, the N /Ar approach underestimates the true volume of the N reservoir, because some (or a lot of) N should exist as lattice- bound NH ions (Li & Keppler, 2014; Li et al., 2013; Mikhail & Sverjensky, FIGURE 4 The abundance of volatile elements in the bulk 2014; Watenphul et al., 2010). Recent experimental data for the silicate Earth relative to the abundances in carbonaceous chondrites partitioning of nitrogen in ferromagnesian minerals show the upper (modified using data from Marty, 2012; and Halliday, 2013) [Colour mantle (<250 km depth) can store 20–50 times more nitrogen figure can be viewed at wileyonlinelibrary.com] ZERKLE and MIKHaIL 348       than the present- day atmosphere (Li et al., 2013), and preliminary Modeling studies of greenhouse warming on the early Earth data suggest the transition zone could store even more (Yoshioka, have proposed elevated pN in the Archean as a solution to the Faint Wiedenbeck, Shcheka, & Keppler, 2016). Therefore, if saturated Young Sun paradox (Airapetian, Glocer, Grono,ff Hebrard, & Danchi, (which is unlikely), then the upper mantle alone can enable the BSE 2016; Goldblatt et al., 2009); however, there is limited evidence to nitrogen abundance to match the C/N ratio of carbonaceous chon- support the suggestion that the Archean had a higher atmospheric drites (shown on Figure 4). pN than the present day. Fossilized raindrop imprints from ~2.7 Ga These datasets and thermodynamic models strongly imply the allow for air density of less than 2 bar, but suggest it was likely less existence of a deep mantle- based nitrogen reservoir. Thus, contrary than 1.1 bar (Som, Catling, Harnmeijer, Polivka, & Buick, 2012; but to previous assumptions, it is now clear that the mantle, and not see Kavanagh & Goldblatt, 2015, for a different interpretation). the atmosphere, could form the largest nitrogen reservoir on Earth Nishizawa, Sano, Ueno, and Marayama (2007) placed an upper limit (Goldblatt et al., 2009; Mikhail & Howell, 2016; Palya, Buick, & Bebout, of 3.3 times the modern N / Ar on the ~3.5 Ga atmosphere based 2011). Various authors have aemp tt ted to provide calculated/assumed on fluid inclusions preserved in hydrothermal quartz, but the ap- reservoir mass fractions for nitrogen in the core, silicate Earth, and proach of Nishizawa et al. (2007) provides no lower limit. Therefore, the atmosphere (Bebout et al., 2013; Dalou et al. 2016; Goldblatt the Archean pN could have been much less than this maximum et al., 2009; Johnson & Goldblatt, 2015; Marty, Zimmermann, Pujol, estimate. Burgess, & Philippot, 2013; Palya et al., 2011); however, these esti- The notion of elevated Archean pN gains some support from in- mates all vary significantly, and there is currently no consensus on the direct evidence, in the form of calculated surface- interior nitrogen flux relative distributions. estimates for the modern Earth system (Barry & Hilton, 2016; Busigny et al., 2011). These studies argue for plate tectonics in the present having a net in- gassing flux of nitrogen to the mantle, despite the 3.3 | Variations in atmospheric pN over mantle wedge being too oxidizing to stabilize ammonium (Figure 2). geologic time This requires that the subducted nitrogen does not enter the melt Direct data for the partial pressure of atmospheric N over time are or fluid phase and is instead retained in the potassium- bearing min- limited, but the majority of available data support lower pN in the erals in the downgoing slab. The pathways for this are theoretically Archean compared to the 0.79 bar of N in the modern atmosphere. well established, whereby NH is transported into the mantle as a 2 4 For example, Marty et al. (2013) used the N / Ar systematics from lattice- bound constituent in potassium- bearing minerals that vary with fluid inclusions trapped in ~3.0 to 3.5 Ga hydrothermal quartz to sug- increasing depth (Harlow & Davies, 2004). These minerals collectively gest the partial pressure of N of the Archean atmosphere could not form a mineralogical conveyor belt for the transfer of nitrogen from exceed 1.1 bar and could be as low as 0.5 bar. More recently, Som the surface to the lowermost mantle (Harlow & Davies, 2004), but + + et al. (2016) used the size distribution of gas bubbles in basaltic lavas the absence of the exchange coefficients for NH /K for potassium- assumed to have solidified at sea level to conclude the atmospheric bearing minerals means no quantitative assumptions can be made at pressure was 0.23 ± 0.23 (2σ) bar at ~2.7 Ga. In support of these this stage. Nonetheless, it is plausible that the aforementioned pro- empirical data, the surface- interior nitrogen flux estimates of Fischer cesses would result in the overall surficial nitrogen reservoir being et al. (2002) suggest plate tectonics (in the present) have a net outgas- depleted through time, and the mantle abundance of nitrogen would sing flux of nitrogen into the atmosphere. be therefore increasing. FIGURE 5 Conceptual models for the mass of nitrogen in Earth’s atmosphere through time. The black dashed line represents the present- day mass of nitrogen in Earth’s atmosphere (see text for details). Both time and mass are arbitrary as this is a suite of conceptual models [Colour figure can be viewed at wileyonlinelibrary.com] ZERKLE and MIKHaIL       349 3.4 | The current state of confusion (aka, 3.4.2 | Scenario #2: Atmospheric pN has increased Schrodinger’s nitrogen cycle) over geologic time Given the uncertainties described above, a complete description of On the other hand, a relatively lower pN for the Archean atmosphere the geobiological nitrogen cycle will require solutions for the following is in line with an interplanetary model proposed to explain an enrich- outstanding questions: (i) a consensus for the fluxes of nitrogen into ment of nitrogen over the primordial noble gases in Earth’s atmos- and out of the mantle, and how these relate to the surficial nitrogen phere relative to the atmospheres on the other sampled planets that cycle, and (ii) the validity of the proposed missing nitrogen conun- are devoid of subduction zone plate tectonics (e.g., Mars and Venus; drum. We suggest that there are three plausible scenarios to recon- Mikhail & Sverjensky, 2014). At present, subduction zones inject oxi- cile these issues within the geobiological nitrogen cycle over Earth’s dizing material into the mantle wedge above the downgoing slab; at 4.6- billion-y ear history, notably that atmospheric pN has changed these redox conditions >QFM, thermodynamic calculations predict unidirectionally (either increased or decreased) over geological time oxidation of NH to N (Figure 2). Because this N is neutrally charged 4 2 2 (Figure 5, conceptual model 1), or the direction of the nitrogen abun- and highly volatile, it is therefore degassed to the atmosphere. This dance of the atmosphere took a dramatic deflection following the model predicts Earth’s arc systems should degas more nitrogen than Great Oxidation Event (Figure 5, conceptual model 2). mid- ocean ridge and hot spot volcanism, consistent with observa- Given the dearth of relevant data, it is impossible to rule out mul- tions (e.g., Hilton, Fischer, & Marty, 2002). In addition, the depend- tidirectional changes in pN over geologic time (Figure 5, conceptual ence of this N production on subduction can explain Earth’s higher 2 2 36 20 model 3), but there is currently no theoretical support or potential atmospheric N / Ar and N / Ne ratios relative to the Martian and 2 2 mechanism for such variations. Conceptual model 2 is exciting and Venusian atmospheres. is mechanistically feasible because of the disparate compatibilities of Furthermore, if the Archean atmospheric mass was below pres- oxidized and reduced nitrogen, as described above. However, for con- ent levels, then we can explain its increase over time by assuming 36 20 ceptual model 2 to be true, then the nitrogen cycle has experienced it must have started with N / Ar and N / Ne ratios similar to 2 2 unidirectional change in both directions, with a major turning point at Mars and Venus. Mikhail and Sverjensky (2014) applied an empir- the GOE. In the following, we explore the geobiological implications of ical nitrogen flux from the Central American volcanic arc system these three scenarios. (from Fischer et al., 2002) and amplified it to represent the global flux (factor of 20 or 10, respectively). Following this methodology, 36 20 the degree of Earth’s atmospheric N / Ar and N / Ne enrich- 2 2 3.4.1 | Scenario #1: Atmospheric pN has decreased ment relative to the atmospheres around Mars and Venus can be over geologic time reproduced over a time period of only 1–2 Ga following the onset If atmospheric pN was relatively higher in the Archean, this could have of subduction (Mikhail & Sverjensky, 2014). However, we should resulted in a greater supply of abiotically fixed nitrogen from the at- specify that this time frame more likely reflects the time period 3+ mosphere than previously estimated (Navarro- Gonzalez et al., 2001). A from which subduction zones began injecting oxidants, like Fe 6+ higher abiotic flux of nitrogen into the biosphere on the early Earth could or S into the mantle (Kelley & Cottrell, 2009), and not simply the have allowed for a much later evolution of N fixation, supporting some onset of subduction. phylogenetic reconstructions and molecular clock data (Boyd, Anbar, This scenario would suggest that an increase in atmospheric pN et al., 2011; Sanchez- Baracaldo, Ridgwell, & Raven, 2014). A decrease over geological time was mirrored by an increase in the burial of ni- in atmospheric pN over geologic time would also follow from our es- trogen in sediments (Figure 3). A positive coupling implies that the timates of enhanced burial of sedimentary nitrogen over geologic time- biosphere could have directly responded to changes in pN caused by scales (Figure 3). A correlation between nitrogen burial and atmospheric progressive degassing of the mantle. As the atmospheric N reservoir pN would suggest that the biosphere could have directly driven changes is orders of magnitude larger than the biosphere, the role of pN in 2 2 in pN via the drawdown of nitrogen from the atmosphere, effectively regulating primary productivity over geologic timescales is generally forming an increasingly efficient geobiological pump of nitrogen from the not considered, assuming an infinite supply for biological N fixation. atmosphere into the sediments, for subsequent storage in the deep Earth. However, it is unclear how abiotic atmospheric sources of fixed nitro- Notably, the scarcity of data available for how these processes, gen (particularly important for early life) could have scaled with pN and the dynamic nitrogen cycle, have interacted over geologic time (Kasting & Siefert, 2001; Navarro- Gonzalez et al., 2001); if pN was means it is impossible to determine whether the global nitrogen cycle very low in the Archean, this could mean even higher levels of nitrogen is currently in equilibrium. Therefore, if a progressive drawdown of N stress and an instantaneous requirement for the evolution of N fixa- 2 2 remained unbalanced by mantle degassing (e.g., Busigny et al., 2011), tion alongside the early biosphere (Stüeken et al., 2015; Weiss et al., over geologic timescales this geobiological nitrogen pump could be 2016). Furthermore, if N outgassing increased aerft the GOE (as dis- progressively depleting Earth’s atmosphere, with currently unexplored cussed below), it could mean that abiotic sources became enhanced consequences for the climate and biogeochemical evolution of a in the early Proterozoic, potentially alleviating some of the biological future Earth system. nitrogen stress proposed for the boring billion. ZERKLE and MIKHaIL 350       toward a deeper connection between biogeochemistry, mantle petrol- 3.4.3 | Scenario #3: Atmospheric pN underwent a ogy, and geodynamics. For example, additional thermodynamic and major turning point during the GOE experimental constraints on N speciation under relevant deep Earth Either in line with or independent of Scenario #2 above, the Great conditions are warranted, but these data are only relevant if the input Oxidation Event could have driven a relative increase in pN by al- (sourced primarily from biology) is considered. The geobiological nitro- tering the speciation and partitioning of nitrogen in subducting gen puzzle will only be solved by considering the biosphere as in-ti sediments. This follows because the speciation and partitioning of ni- mately connected with the geosphere, and vice versa. We therefore put trogen are redox- sensitive, as discussed in section 2.2. Therefore, the this challenge to the Geobiology community, to don your hard hats and relative abundance of nitrogen degassed out of the mantle over time delve into Earth’s interior (accompanied by your hard- rock colleagues). must have changed before and after the GOE, because the oxidizing potential of the material subducted (oceanic sediments and altered A CKNO WLEDGMENT S oceanic crust) must have differed. In particular, post- GOE the oxida- tion state of the mantle overlying the slabs would become too oxidiz- AZ acknowledges Natural Environmental Research Council Fellowship ing to stabilize ammonic nitrogen, and molecular nitrogen would be NE/H016805 for financial support. The authors would also like to favored (Figure 2). As inert N molecules are highly volatile and highly thank M. Claire and E. Stüeken for valuable discussions and P. Barry incompatible in all mineral phases, this molecular N would be re- for sharing his modeling data. leased as a gas- phase to the atmosphere, a concept not quantitatively incorporated into recent flux models (Barry & Hilton, 2016; Busigny REFERENCES et al., 2011; Fischer et al., 2002). Therefore, we propose (on a global Airapetian, V. S., Glocer, A., Grono,ff G., Hebrard, E., & Danchi, W. 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The geobiological nitrogen cycle: From microbes to the mantle

Zerkle, A. L.; Mikhail, S.
Geobiology , Volume 15 (3) – May 1, 2017
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Abstract

Centre for Exoplanet Science, University of St Andrews, St Andrews, Fife, UK Nitrogen forms an integral part of the main building blocks of life, including DNA, RNA, and proteins. N is the dominant gas in Earth’s atmosphere, and nitrogen is stored in Correspondence 2 A. L. Zerkle, School of Earth & Environmental all of Earth’s geological reservoirs, including the crust, the mantle, and the core. As Sciences and Centre for Exoplanet Science, such, nitrogen geochemistry is fundamental to the evolution of planet Earth and the University of St Andrews, St Andrews, Fife, UK. life it supports. Despite the importance of nitrogen in the Earth system, large gaps Email: az29@st-andrews.ac.uk remain in our knowledge of how the surface and deep nitrogen cycles have evolved Funding information over geologic time. Here, we discuss the current understanding (or lack thereof) for Natural Environmental Research Council how the unique interaction of biological innovation, geodynamics, and mantle petrol- Fellowship, Grant/Award Number: NE/ H016805 ogy has acted to regulate Earth’s nitrogen cycle over geologic timescales. In particular, we explore how temporal variations in the external (biosphere and atmosphere) and internal (crust and mantle) nitrogen cycles could have regulated atmospheric pN . We consider three potential scenarios for the evolution of the geobiological nitrogen cycle over Earth’s history: two in which atmospheric pN has changed unidirectionally (in- creased or decreased) over geologic time and one in which pN could have taken a dramatic deflection following the Great Oxidation Event. It is impossible to discrimi- nate between these scenarios with the currently available models and datasets. However, we are optimistic that this problem can be solved, following a sustained, open- minded, and multidisciplinary effort between surface and deep Earth communities. 1  |  INTR ODUCTION The chemistry of Earth’s atmosphere is in a constant state of dis- equilibrium due to atmospheric photochemistry, life’s collective me- Understanding the nitrogen cycle is part of a dynamic geobiological tabolisms, chemical weathering, and the large- scale geochemical fluxes puzzle, for which the ultimate goal is illuminating the mechanics re- imposed by plate tectonics and related volcanism (Bebout, Fogel, & sponsible for the development of habitability on Earth and on other Cartigny, 2013). However, atmospheric chemistry is not a constant planets, in our solar system and beyond. For example, nitrogen is a key though time (Barry & Hilton, 2016; Mikhail & Sverjensky, 2014). The element in the structure of amino acids, proteins, nucleic acids, and most dramatic geochemical transition since the formation of the at- other molecules vital to life and is also the dominant component of mosphere was biological rather than geological in nature. Sometime in Earth’s atmosphere. In addition, the oxidation of ammonic nitrogen the mid- to late Archean (e.g., Farquhar, Zerkle, & Bekker, 2011), mi- (NH ) in the mantle has been proposed as a source of liquid water crobial life developed the ability to perform oxygenic photosynthesis, to the early Earth (Li & Keppler, 2014), and N could have played an which uses energy from the sun and raw materials extracted from the important role in maintaining Earth’s surface above the freezing point geosphere (CO + H O) to generate energy, construct essential building 2 2 of water in the presence of the faint young sun (e.g., Goldbla tt et al., materials, and releases oxygen in a gas phase (O ) as a waste product. 2009). Over time this biological revelation cumulatively oxygenated Earth’s This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2017 The Authors Geobiology Published by John Wiley & Sons Ltd Geobiology. 2017;15:343–352. wileyonlinelibrary.com/journal/gbi     343 Denitrification remin. Upwelling ZERKLE and MIKHaIL 344       surface. The result is that Earth’s atmosphere became highly reactive, NO to N ) and anaerobic ammonium oxidation (anammox, the oxi- 3 2 + − unlike the atmospheres of Mars and Venus which are still dominated by dation of NH to N using NO ; Dalsgaard, Thamdrup, & Canfield, 4 2 2 unreactive gases (CO + N ). The combination of a uniquely reactive- 2005). These processes, which result in the loss of fixed N from the 2 2 gas- rich atmosphere and hydrosphere, coupled with subduction zone biosphere, occur in soils, marine sediments, and oxygen minimum plate tectonics, means that Earth injects oxidizing material into a rel- zones, completing the biological nitrogen cycle (Figure 1). atively reduced mantle (Frost & Mccammon, 2008; Kelley & Cottrell, All life requires N in a reduced form, which can either be taken up 2009). This phenomenon is seemingly unique because such biological directly as ammonium or enzymatically reduced during nitrate assimi- and tectonic processes are only known to occur on Earth. Here, we lation. Once assimilated into biomass, organic nitrogen is recycled via compare and contrast current ideas for how this unique interaction of release and re- assimilation of organic N within the surface ocean, or biological innovation, geodynamics, and mantle petrology could have subsequently regenerated during organic maertt remineralization in acted to regulate the geobiological nitrogen cycle over Earth history. sediments. Over geologic timescales, some small amount of fixed nitro- gen can leak out of the biosphere–ocean system and be buried in the sediments, as organic nitrogen or as remineralized ammonium incorpo- 2  |  B A CK GR OUND rated into clays during diagenesis (Schroeder & McLain, 1998). During burial, nitrogen- bearing rocks can undergo metamorphism, which can 2.1 | Surficial nitrogen cycle return a significant fraction of the nitrogen back to the atmosphere Molecular nitrogen in the gas- phase (N ) is the largest surficial res- (e.g., Haendel, Mühle, Nitzsche, Stiehl, & Wand, 1986). The remainder ervoir of nitrogen and comprises around 78% of Earth’s atmosphere. of N entrained within sediments can be subducted, along with nitrogen Atmospheric nitrogen is incorporated into the biosphere via the pro- sequestered into altered oceanic lithosphere as ammonium and organic cess of N fixation, whereby specialized prokaryotes convert this inert species (Busigny, Cartigny, & Philippot, 2011; Halama, Bebout, John, & N gas into biomolecules (as C- NH ) (Figure 1). Nitrogen fixation is an Scambelluri, 2014). This subduction of sediment and altered oceanic 2 2 energetically expensive process which requires 16 ATP to break the lithosphere constitutes the primary flux of surficial N into the deep triply bonded N molecule. N - fixing organisms (termed “diazotrophs”) Earth. 2 2 accomplish this feat by utilizing the nitrogenase metallo- enzyme com- plex, which contains Fe and Mo in its most efficient form. 2.2 | Deep earth nitrogen cycle Nitrogen fixed as ammonium (NH ) is dominantly recycled by the − − biosphere or sequentially oxidized to nitrite (NO ) and nitrate (NO ). Once subducted into the deep Earth, nitrogen has historically been 2 3 Ammonium oxidation (“nitrification”) generally requires molecular considered an unreactive gas in the field of mantle geochemistry, oxygen (Carlucci & Mcnally, 1969). These “oxidized” nitrogen com- owing to the strength of the covalent triple N- bond, and abundance pounds provide an important nutrient source for eukaryotic primary of N in the atmosphere (e.g., Boyd & Pillinger, 1994; Javoy, Pineau, producers. Alternatively, nitrate (and some nitrite) can also be reduced & Delorme, 1986). Consequently, the behavior of nitrogen has tradi- back to ammonium via dissimilatory nitrate reduction to ammonium tionally been assumed to be akin to the unreactive noble gases (e.g., (DNRA), another process that was described fairly recently in the mod- Bergin, Blake, Ciesla, Hirschmann, & Li, 2015; Halliday, 2013; Marty, ern system (Lam et al., 2009). 1995, 2012; Mikhail, Dobosi, Verchovsky, Kurat, & Jones, 2013). Fixed nitrogen can be returned to the atmosphere as N via several However, empirical data show a diverse variety of nitrogen species chemotrophic metabolisms, including denitrification (the reduction of are present in the deep Earth, including molecular N , ammonium, FIGURE 1 Basin- scale model of the N N N N 2 2 2 2 modern marine biogeochemical nitrogen 2 N cycle. The red pathways are anaerobic Fixation Fixation pathways that would have presumably Norg + - + Norg NH NO NH dominated in anoxic Archean environments. 4 3 4 nit. recyc. The blue pathways require oxygen (or Uptake Burial an oxidized nitrogen species) and would presumably have proliferated after the Norg GOE. Note that for simplicity the nitrite - OMZ NH and nitrate pools are shown combined, 4 NO DNRA as NO . Additional abbreviations are as follows: OMZ = oxygen minimum zone NO3 (shown in purple); DNRA = dissimilatory nit. nitrate reduction to ammonium; nit. = NH nitrification; remin. = remineralization; Burial recyc. = recycling [Colour figure can be org viewed at wileyonlinelibrary.com] Anammox ZERKLE and MIKHaIL       345 we must rely on sparse data and predictive thermodynamic models to estimate past N dynamics. 3  |  DISCUSSION 3.1 | Evolution of the biogeochemical N cycle The emergence and evolution of biogeochemical nitrogen cycling over Earth history remains a major question mark in the field of geobiol- ogy (e.g., see recent review by Stüeken, Kipp, Koehler, & Buick, 2016). Abiotic N reduction to ammonium within hydrothermal systems could have supplied fixed nitrogen to an early deep biosphere (Brandes et al., 1998; Nishizawa, Miyazaki, Makabe, Koba, & Takai, 2014). Once an- oxygenic photosynthesis evolved sometime in the Archean, primary productivity would have been most abundant in the surface waters. FIGURE 2 The speciation of aqueous nitrogen at 5 GPa at Dry deposition or fixation by lightning could have provided an abi- 1000°C, calculated in equilibrium with Forsterite and Fayalite using otic supply of nitrogen to the surface oceans from the atmosphere the Deep Earth Water model (from Mikhail & Sverjensky, 2014) [Colour figure can be viewed at wileyonlinelibrary.com] (Navarro- Gonzalez, Mckay, & Mvondo, 2001). However, estimates of a very limited supply of nitrogen from these abiotic sources suggest that diamond (NC ), metallic nitride (Fe N, TiN, BN), and nitro- carbide (for N fixation must have evolved very early in life’s history to support an 3 3 2 comprehensive reviews of nitrogen in the deep Earth, see Bebout, ever- expanding biosphere (Haqq- Misra, Domagal- Goldman, Kasting, & Lazzeri, & Geiger, 2016; and Johnson & Goldblatt, 2015). All of the Kasting, 2008; Kasting & Siefert, 2001; Kharecha, Kasting, & Siefert, aforementioned species of nitrogen behave differently, where their 2005). Phylogenetic reconstructions of genes for the nitrogenase en- behavior can be described as compatible or incompatible to a host zyme support its early emergence (Boyd, Hamilton, & Peters, 2011; mineral phase, depending on charge and radius of the ion and the Fani, Gallo, & Lio, 2000; Raymond, Siefert, Staples, & Blankenship, occupation site in the mineral (Goldschmidt, 1924). For nitrogen in 2004; Weiss et al., 2016), possibly in an anoxic environment (Boyd & the mantle, recent experimentally and theoretically determined equi- Peters, 2013). In addition, the sedimentary δ N record suggests this librium constants have shown that ammonium should dominate over process could have been active as far back as ~3.2 Ga (Stüeken, Buick, molecular nitrogen in aqueous fluids in the uppermost mantle where Guy, & Koehler, 2015). Once N fixation was established, it is generally the redox state (fO ) is buffered below the quartz–fayalite–magnet- assumed that the input of nitrogen to the biosphere could keep pace ite buffer (QFM) (Li & Keppler, 2014; Mikhail & Sverjensky, 2014) with primary productivity as long as no other nutrient (e.g., phospho- (Figure 2). This is a significant insight, because for nitrogen, compat- rus or bioactive trace metals; Tyrrell, 1999; Anbar & Knoll, 2002) was ibility is directly related to speciation: Molecular nitrogen (N ) is limiting. highly incompatible, whereas ammonium (NH ) is likely compatible in As the speciation and microbial cycling of nitrogen are highly redox- potassium- bearing mineral phases (Watenphul, Wunder, & Heinrich, dependent, the biogeochemical nitrogen cycle would have changed 2009) and can dissolve as a trace component in potassium- absent significantly with the progressive oxygenation of Earth surface environ- phases (Li, Wiedenbeck, Shcheka, & Keppler, 2013; Watenphul, ments (e.g., Stüeken et al., 2016). Notably, in Earth’s Archean oceans Wunder, Wirth, & Heinrich, 2010). This is a crucial distinction from before the buildup of significant oxygen, processes involved in the the perspective of the global nitrogen cycle, because nitrogen in the modern N cycle that required molecular oxygen (or the presence of sig- molecular form is likely to be outgassed, while ammonium could be nificant quantities of oxidized N compounds) would have been absent. stored in mineral phases in the deep Earth (Mikhail & Sverjensky, In particular, nitrification, the stepwise oxidation of ammonium to ni- 2014). We explore this concept, and its potential response to changes trite and nitrate, requires at least some free oxygen (Carlucci & Mcnally, in global redox, in the discussion below. 1969). Thus, throughout the Archean and earliest Paleoproterozoic the Because Earth is a dynamic planet with active plate tectonics, nitrogen cycle would likely have consisted of N fixation followed by what goes into the mantle sometimes comes back out, and vice versa. burial and regeneration of NH in sediments (Figure 1). Therefore, the exchange of nitrogen between the surface and inte- Following widespread oxygenation of the marine biosphere during rior is governed by subduction (in- gassing) and volcanism (outgassing), the Great Oxidation Event (GOE) between ~2.4 and 2.3 Ga (e.g., re- and this interplay ultimately controls atmospheric N levels (Cartigny viewed in Farquhar, Zerkle, & Bekker, 2014), the primary N loss path- & Ader, 2003; Dauphas & Marty, 2004; Kerrich & Jia, 2004; Marty ways of denitrification and anammox proliferated to take advantage & Dauphas, 2003a,b). However, the further back one looks in time of the newly available oxidized N compounds (Zerkle et al., 2017). In the less data are available, and there is a predictable dearth of data the redox- stratified oceans that developed during this time period to constrain either the fluxes of nitrogen over geological time, or the (e.g., Poulton, Fralick, & Canfield, 2010; Scott et al., 2011; Zerkle et al., partial pressure of atmospheric nitrogen in the deep past. This means 2017), nitrification of ammonium- rich deep waters was confined to ZERKLE and MIKHaIL 346       the oxic–anoxic interface, with denitrification and anammox occurring a competitive advantage. Many researchers have suggested that N just below. fixation would also have been limited in the Proterozoic oceans, due The expansion of an aerobic N cycle during the GOE is supported to drawdown of bioactive trace metals required for nitrogenase (par- by temporal trends in sedimentary N isotope records, which show ticularly Mo) under widespread sulfidic conditions (Anbar & Knoll, a shift toward more positive δ N values similar to modern marine 2002). Metal limitation experiments with modern N - fixing cyano- values by ~2.3 Ga (Beaumont & Robert, 1999; Zerkle et al., 2017). bacteria suggest that vanishingly little Mo is actually required to sup- Studies of much older sediments (2.5–2.7 Ga) have interpreted tran- port modern rates of diazotrophy (down to ~5 nM; Zerkle, House, sitory increases in δ N as recording a temporary insurgence of oxi- Cox, & Canfield, 2006; Glass, Wolfe- Simon, & Anbar, 2009). Current dative N cycling, potentially related to localized transient increases in estimates of molybdenum concentrations in Precambrian oceans are marine O (Garvin, Buick, Anbar, Arnold, & Kaufman, 2009; Godfrey insufficient to resolve this issue at present (Reinhard, Raiswell, Scott, & Falkowski, 2009; Thomazo, Ader, & Philippot, 2011). These stud- Anbar, & Lyons, 2009; Scott et al., 2008). However, records of molyb- ies suggest that the aerobic N pathways could have evolved imme- denum in shales suggest that marine molybdenum levels rose to near diately following oxygenic photosynthesis, to take advantage of the modern levels at the end of the Neoproterozoic with enhanced oxida- newly available free oxygen in highly productive coastal environments. tive weathering during a second rise in atmospheric O (Sahoo et al., However, the isotope eect ff associated with these N loss pathways 2012), potentially further enhancing global N fixation rates. would only have been expressed once nitrite/nitrate was available at As the delivery of nitrogen to the sediments is intimately sufficient levels that their quantitative removal from the ocean did linked to the biosphere and dependent on redox and other en- not occur. Therefore, the shift toward more positive δ N values by vironmental parameters, the burial of nitrogen over geologic ~2.3 Ga (Zerkle et al., 2017) represents a turning point in the balance time (and thus its flux into the mantle) would have changed in − − of NO loss to NO supply, rather than the exact timing of when the response to these changes in the biogeochemical nitrogen cycle. 3 3 oxidative N cycle first evolved. Using conservative estimates for the timing of major biological The persistence of a deep anoxic water column after the emer- and geochemical innovations, we can propose a rough timeline gence of the aerobic N cycle could have had a dramatic eect ff on for changes in the burial of N into marine sediments over geologic the abundance of fixed nitrogen in the world’s oceans. Massive losses time (Figure 3). Nitrogen burial is thought to be generally driven of fixed nitrogen via denitrification and anammox are predicted to by changes in carbon burial over time (e.g., Berner, 2006), which have occurred during periods of deepwater anoxia (Canfield, Rosing, itself plays an important role in regulating Earth surface redox & Bjerrum, 2006; Fennel, Follows, & Falkowski, 2005), potentially conditions (e.g., Krissansen-Totton, Buick, & Catling, 2015). For limiting the availability of fixed inorganic nitrogen for primary produc- this calculation, we used the productivity estimates of Canfield, tion. These researchers suggest that such nitrogen limitation could Glazer and Falkowsk (2010) for primary production based on an have reduced the burial of organic carbon, and the resulting accumu- evolutionary progression of anoxygenic photoautotrophy, oxy- lation of atmospheric oxygen, eectiv ff ely hindering the evolution of genic photoautotrophy, and eukaryotic photoautotrophy. We uti- eukaryotes, as well as the continued oxygenation of Earth’s surface lized a constant burial rate of 10% total biomass (similar to the environments. Nitrogen isotope records from the Mesoproterozoic modern; Gruber, 2008) with a constant Redfield ratio of 6:1 (C:N). support nitrogen limitation, particularly within open ocean settings We used denitrification levels estimated from modern marine N (Stüeken, 2013). balances (e.g., Canfield et al., 2010; Gruber, 2008). The biggest The mid- Proterozoic nitrogen limitation hypothesis is predicated on unknown in this calculation is when coupled nitrification/denitri- the assumptions that the majority of primary productivity was occurring fication proliferated and how rates of denitrification responded via oxygenic photosynthesis in the surface ocean and that nitrogen fixa- to changes in ocean chemistry throughout the Proterozoic (as dis- tion could not keep pace with the fixed N loss (and the delivery of other cussed above). For this calculation, we assumed 25% of modern nutrients) to fuel this primary productivity. The evolution of oxygenic denitrification levels early in the GOE, and an increase to 130% photosynthesis in the late Archean would certainly have resulted in a associated with the subsequent buildup of a nitrate reservoir marked increase in global rates of primary production (Canfield et al., in a largely anoxic ocean, with large error bars to highlight this 2006). Johnston, Wolfe- Simon, Pearson, and Knoll (2009) point out uncertainty. Finally, we calculated changes in N fixation rates that anoxygenic photoautotrophs could also have made an important with enhanced molybdenum delivery during the Neoproterozoic contribution to primary productivity in the redox- stratified continen- Oxygenation Event (NOE) as a switch from molybdenum- limited tal margins that that seemingly dominated for much of the Proterozoic to modern N fixation rates, based on the experiments of Zerkle (e.g., Poulton et al., 2010; Sco tt et al., 2011). Primary producers in mar- et al. (2006). Note that this calculation does not consider any sig- ginal sulfidic zones could have had direct access to upwelling nutrients, nificant loss of nitrogen from the sediments during diagenesis or including ammonium, before it reached the redox interface and was lost metamorphic reactions prior to subduction. Notably, this scenario to nitrification–denitrification and anammox reactions. for changes in nitrogen burial over time predicts a progressive Consumption of upwelling ammonium by anoxygenic phototro- increase in the delivery of nitrogen to the deep Earth via sub- phs could have further contributed to the fixed nitrogen deficit in duction (with the exception of the possible mid- Proterozoic mini- surface waters, such that N - fixing organisms in the photic zone had mum) following an ever- increasingly efficient biosphere. 2 % Modern N burial ZERKLE and MIKHaIL       347 GOE NOE - - Low [NO ] High [NO ] Low [Mo] High [Mo] 3 3 Oxygenic photosynthesis Anoxygenic photosynthesis Origin of life Archean Proterozoic Phan. 4000 2500 542 0 Time (Ma) FIGURE 3 Estimated burial flux of nitrogen through time, following calculations described in the text [Colour figure can be viewed at wileyonlinelibrary.com] and Kr—elements that are far more akin to Xe in terms of geochemi- 3.2 | The missing nitrogen conundrum cal behavior, and in the case of Kr, mass. Another explanation is that Our understanding of the evolution of the deep Earth nitrogen cycle there exists a hidden nitrogen reservoir in the deep Earth, inferred to and the relevant nitrogen reservoirs is even less well constrained. be the core or unspecified deep mantle domain (Barry & Hilton, 2016; One puzzle often cited is the “missing nitrogen conundrum,” which Halliday, 2013; Marty, 2012). This reservoir is unlikely to be the core follows because the abundance of nitrogen in the bulk silicate Earth because carbon is more siderophile than nitrogen (Dalou, Hirschmann, (BSE) appears to be significantly lower than that of other volatile von der Handt, Mosenfelder, & Armstrong, 2016); therefore, a mantle elements (Figure 4). The most striking feature of these data is the reservoir is more in line with what is known about the partitioning of depletions shown for Xe and N, which could mean that these two el- carbon and nitrogen during core formation. Furthermore, stable iso- ements with contrasting behaviors and masses were both lost early tope data for diamonds show that nitrogen is subducted back into in Earth’s history (Bergin et al., 2015) without also depleting Ne, Ar, the deep mantle, implying nitrogen retention during subduction to at least the minimum depth of diamond stability (≥150 km; Mikhail et al., 2014) and possibly into the lower mantle (≥660 km; Palot, Cartigny, Harris, Kaminsky, & Stachel, 2012). This requires a mechanism to transport nitrogen beyond the mantle wedge. Note that Figure 4 is derived by summing up the assumed abun- dance of nitrogen in the BSE with the surficial reservoir; however, these values were calculated using N /Ar ratios, which is now known to be inaccurate for the majority of the mantle. In particu- lar, the N /Ar approach underestimates the true volume of the N reservoir, because some (or a lot of) N should exist as lattice- bound NH ions (Li & Keppler, 2014; Li et al., 2013; Mikhail & Sverjensky, FIGURE 4 The abundance of volatile elements in the bulk 2014; Watenphul et al., 2010). Recent experimental data for the silicate Earth relative to the abundances in carbonaceous chondrites partitioning of nitrogen in ferromagnesian minerals show the upper (modified using data from Marty, 2012; and Halliday, 2013) [Colour mantle (<250 km depth) can store 20–50 times more nitrogen figure can be viewed at wileyonlinelibrary.com] ZERKLE and MIKHaIL 348       than the present- day atmosphere (Li et al., 2013), and preliminary Modeling studies of greenhouse warming on the early Earth data suggest the transition zone could store even more (Yoshioka, have proposed elevated pN in the Archean as a solution to the Faint Wiedenbeck, Shcheka, & Keppler, 2016). Therefore, if saturated Young Sun paradox (Airapetian, Glocer, Grono,ff Hebrard, & Danchi, (which is unlikely), then the upper mantle alone can enable the BSE 2016; Goldblatt et al., 2009); however, there is limited evidence to nitrogen abundance to match the C/N ratio of carbonaceous chon- support the suggestion that the Archean had a higher atmospheric drites (shown on Figure 4). pN than the present day. Fossilized raindrop imprints from ~2.7 Ga These datasets and thermodynamic models strongly imply the allow for air density of less than 2 bar, but suggest it was likely less existence of a deep mantle- based nitrogen reservoir. Thus, contrary than 1.1 bar (Som, Catling, Harnmeijer, Polivka, & Buick, 2012; but to previous assumptions, it is now clear that the mantle, and not see Kavanagh & Goldblatt, 2015, for a different interpretation). the atmosphere, could form the largest nitrogen reservoir on Earth Nishizawa, Sano, Ueno, and Marayama (2007) placed an upper limit (Goldblatt et al., 2009; Mikhail & Howell, 2016; Palya, Buick, & Bebout, of 3.3 times the modern N / Ar on the ~3.5 Ga atmosphere based 2011). Various authors have aemp tt ted to provide calculated/assumed on fluid inclusions preserved in hydrothermal quartz, but the ap- reservoir mass fractions for nitrogen in the core, silicate Earth, and proach of Nishizawa et al. (2007) provides no lower limit. Therefore, the atmosphere (Bebout et al., 2013; Dalou et al. 2016; Goldblatt the Archean pN could have been much less than this maximum et al., 2009; Johnson & Goldblatt, 2015; Marty, Zimmermann, Pujol, estimate. Burgess, & Philippot, 2013; Palya et al., 2011); however, these esti- The notion of elevated Archean pN gains some support from in- mates all vary significantly, and there is currently no consensus on the direct evidence, in the form of calculated surface- interior nitrogen flux relative distributions. estimates for the modern Earth system (Barry & Hilton, 2016; Busigny et al., 2011). These studies argue for plate tectonics in the present having a net in- gassing flux of nitrogen to the mantle, despite the 3.3 | Variations in atmospheric pN over mantle wedge being too oxidizing to stabilize ammonium (Figure 2). geologic time This requires that the subducted nitrogen does not enter the melt Direct data for the partial pressure of atmospheric N over time are or fluid phase and is instead retained in the potassium- bearing min- limited, but the majority of available data support lower pN in the erals in the downgoing slab. The pathways for this are theoretically Archean compared to the 0.79 bar of N in the modern atmosphere. well established, whereby NH is transported into the mantle as a 2 4 For example, Marty et al. (2013) used the N / Ar systematics from lattice- bound constituent in potassium- bearing minerals that vary with fluid inclusions trapped in ~3.0 to 3.5 Ga hydrothermal quartz to sug- increasing depth (Harlow & Davies, 2004). These minerals collectively gest the partial pressure of N of the Archean atmosphere could not form a mineralogical conveyor belt for the transfer of nitrogen from exceed 1.1 bar and could be as low as 0.5 bar. More recently, Som the surface to the lowermost mantle (Harlow & Davies, 2004), but + + et al. (2016) used the size distribution of gas bubbles in basaltic lavas the absence of the exchange coefficients for NH /K for potassium- assumed to have solidified at sea level to conclude the atmospheric bearing minerals means no quantitative assumptions can be made at pressure was 0.23 ± 0.23 (2σ) bar at ~2.7 Ga. In support of these this stage. Nonetheless, it is plausible that the aforementioned pro- empirical data, the surface- interior nitrogen flux estimates of Fischer cesses would result in the overall surficial nitrogen reservoir being et al. (2002) suggest plate tectonics (in the present) have a net outgas- depleted through time, and the mantle abundance of nitrogen would sing flux of nitrogen into the atmosphere. be therefore increasing. FIGURE 5 Conceptual models for the mass of nitrogen in Earth’s atmosphere through time. The black dashed line represents the present- day mass of nitrogen in Earth’s atmosphere (see text for details). Both time and mass are arbitrary as this is a suite of conceptual models [Colour figure can be viewed at wileyonlinelibrary.com] ZERKLE and MIKHaIL       349 3.4 | The current state of confusion (aka, 3.4.2 | Scenario #2: Atmospheric pN has increased Schrodinger’s nitrogen cycle) over geologic time Given the uncertainties described above, a complete description of On the other hand, a relatively lower pN for the Archean atmosphere the geobiological nitrogen cycle will require solutions for the following is in line with an interplanetary model proposed to explain an enrich- outstanding questions: (i) a consensus for the fluxes of nitrogen into ment of nitrogen over the primordial noble gases in Earth’s atmos- and out of the mantle, and how these relate to the surficial nitrogen phere relative to the atmospheres on the other sampled planets that cycle, and (ii) the validity of the proposed missing nitrogen conun- are devoid of subduction zone plate tectonics (e.g., Mars and Venus; drum. We suggest that there are three plausible scenarios to recon- Mikhail & Sverjensky, 2014). At present, subduction zones inject oxi- cile these issues within the geobiological nitrogen cycle over Earth’s dizing material into the mantle wedge above the downgoing slab; at 4.6- billion-y ear history, notably that atmospheric pN has changed these redox conditions >QFM, thermodynamic calculations predict unidirectionally (either increased or decreased) over geological time oxidation of NH to N (Figure 2). Because this N is neutrally charged 4 2 2 (Figure 5, conceptual model 1), or the direction of the nitrogen abun- and highly volatile, it is therefore degassed to the atmosphere. This dance of the atmosphere took a dramatic deflection following the model predicts Earth’s arc systems should degas more nitrogen than Great Oxidation Event (Figure 5, conceptual model 2). mid- ocean ridge and hot spot volcanism, consistent with observa- Given the dearth of relevant data, it is impossible to rule out mul- tions (e.g., Hilton, Fischer, & Marty, 2002). In addition, the depend- tidirectional changes in pN over geologic time (Figure 5, conceptual ence of this N production on subduction can explain Earth’s higher 2 2 36 20 model 3), but there is currently no theoretical support or potential atmospheric N / Ar and N / Ne ratios relative to the Martian and 2 2 mechanism for such variations. Conceptual model 2 is exciting and Venusian atmospheres. is mechanistically feasible because of the disparate compatibilities of Furthermore, if the Archean atmospheric mass was below pres- oxidized and reduced nitrogen, as described above. However, for con- ent levels, then we can explain its increase over time by assuming 36 20 ceptual model 2 to be true, then the nitrogen cycle has experienced it must have started with N / Ar and N / Ne ratios similar to 2 2 unidirectional change in both directions, with a major turning point at Mars and Venus. Mikhail and Sverjensky (2014) applied an empir- the GOE. In the following, we explore the geobiological implications of ical nitrogen flux from the Central American volcanic arc system these three scenarios. (from Fischer et al., 2002) and amplified it to represent the global flux (factor of 20 or 10, respectively). Following this methodology, 36 20 the degree of Earth’s atmospheric N / Ar and N / Ne enrich- 2 2 3.4.1 | Scenario #1: Atmospheric pN has decreased ment relative to the atmospheres around Mars and Venus can be over geologic time reproduced over a time period of only 1–2 Ga following the onset If atmospheric pN was relatively higher in the Archean, this could have of subduction (Mikhail & Sverjensky, 2014). However, we should resulted in a greater supply of abiotically fixed nitrogen from the at- specify that this time frame more likely reflects the time period 3+ mosphere than previously estimated (Navarro- Gonzalez et al., 2001). A from which subduction zones began injecting oxidants, like Fe 6+ higher abiotic flux of nitrogen into the biosphere on the early Earth could or S into the mantle (Kelley & Cottrell, 2009), and not simply the have allowed for a much later evolution of N fixation, supporting some onset of subduction. phylogenetic reconstructions and molecular clock data (Boyd, Anbar, This scenario would suggest that an increase in atmospheric pN et al., 2011; Sanchez- Baracaldo, Ridgwell, & Raven, 2014). A decrease over geological time was mirrored by an increase in the burial of ni- in atmospheric pN over geologic time would also follow from our es- trogen in sediments (Figure 3). A positive coupling implies that the timates of enhanced burial of sedimentary nitrogen over geologic time- biosphere could have directly responded to changes in pN caused by scales (Figure 3). A correlation between nitrogen burial and atmospheric progressive degassing of the mantle. As the atmospheric N reservoir pN would suggest that the biosphere could have directly driven changes is orders of magnitude larger than the biosphere, the role of pN in 2 2 in pN via the drawdown of nitrogen from the atmosphere, effectively regulating primary productivity over geologic timescales is generally forming an increasingly efficient geobiological pump of nitrogen from the not considered, assuming an infinite supply for biological N fixation. atmosphere into the sediments, for subsequent storage in the deep Earth. However, it is unclear how abiotic atmospheric sources of fixed nitro- Notably, the scarcity of data available for how these processes, gen (particularly important for early life) could have scaled with pN and the dynamic nitrogen cycle, have interacted over geologic time (Kasting & Siefert, 2001; Navarro- Gonzalez et al., 2001); if pN was means it is impossible to determine whether the global nitrogen cycle very low in the Archean, this could mean even higher levels of nitrogen is currently in equilibrium. Therefore, if a progressive drawdown of N stress and an instantaneous requirement for the evolution of N fixa- 2 2 remained unbalanced by mantle degassing (e.g., Busigny et al., 2011), tion alongside the early biosphere (Stüeken et al., 2015; Weiss et al., over geologic timescales this geobiological nitrogen pump could be 2016). Furthermore, if N outgassing increased aerft the GOE (as dis- progressively depleting Earth’s atmosphere, with currently unexplored cussed below), it could mean that abiotic sources became enhanced consequences for the climate and biogeochemical evolution of a in the early Proterozoic, potentially alleviating some of the biological future Earth system. nitrogen stress proposed for the boring billion. ZERKLE and MIKHaIL 350       toward a deeper connection between biogeochemistry, mantle petrol- 3.4.3 | Scenario #3: Atmospheric pN underwent a ogy, and geodynamics. For example, additional thermodynamic and major turning point during the GOE experimental constraints on N speciation under relevant deep Earth Either in line with or independent of Scenario #2 above, the Great conditions are warranted, but these data are only relevant if the input Oxidation Event could have driven a relative increase in pN by al- (sourced primarily from biology) is considered. The geobiological nitro- tering the speciation and partitioning of nitrogen in subducting gen puzzle will only be solved by considering the biosphere as in-ti sediments. This follows because the speciation and partitioning of ni- mately connected with the geosphere, and vice versa. We therefore put trogen are redox- sensitive, as discussed in section 2.2. Therefore, the this challenge to the Geobiology community, to don your hard hats and relative abundance of nitrogen degassed out of the mantle over time delve into Earth’s interior (accompanied by your hard- rock colleagues). must have changed before and after the GOE, because the oxidizing potential of the material subducted (oceanic sediments and altered A CKNO WLEDGMENT S oceanic crust) must have differed. In particular, post- GOE the oxida- tion state of the mantle overlying the slabs would become too oxidiz- AZ acknowledges Natural Environmental Research Council Fellowship ing to stabilize ammonic nitrogen, and molecular nitrogen would be NE/H016805 for financial support. The authors would also like to favored (Figure 2). As inert N molecules are highly volatile and highly thank M. Claire and E. Stüeken for valuable discussions and P. Barry incompatible in all mineral phases, this molecular N would be re- for sharing his modeling data. leased as a gas- phase to the atmosphere, a concept not quantitatively incorporated into recent flux models (Barry & Hilton, 2016; Busigny REFERENCES et al., 2011; Fischer et al., 2002). Therefore, we propose (on a global Airapetian, V. S., Glocer, A., Grono,ff G., Hebrard, E., & Danchi, W. 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Geobiology – Wiley

Published: May 1, 2017

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