Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment

Tamara Martin-Pozas; Jose Luis Gonzalez-Pimentel; Valme Jurado; Leonila Laiz; Juan Carlos Cañaveras; Angel Fernandez-Cortes; Soledad Cuezva; Sergio Sanchez-Moral; Cesareo Saiz-Jimenez

doi:10.3390/applbiosci2020014

Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment

Martin-Pozas, Tamara;Gonzalez-Pimentel, Jose Luis;Jurado, Valme;Laiz, Leonila;Cañaveras, Juan Carlos;Fernandez-Cortes, Angel;Cuezva, Soledad;Sanchez-Moral, Sergio;Saiz-Jimenez, Cesareo 2023-05-06 00:00:00 Review Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment 1 , † 2 , † 3 3 4 Tamara Martin-Pozas , Jose Luis Gonzalez-Pimentel , Valme Jurado , Leonila Laiz , Juan Carlos Cañaveras , 5 6 1 3 , Angel Fernandez-Cortes , Soledad Cuezva , Sergio Sanchez-Moral and Cesareo Saiz-Jimenez * Museo Nacional de Ciencias Naturales, MNCN-CSIC, 28006 Madrid, Spain Centro Andaluz de Biologia del Desarrollo (CABD, UPO-CSIC-JA), Facultad de Ciencias Experimentales, Departamento de Genetica, Universidad Pablo de Olavide, 41013 Sevilla, Spain Instituto de Recursos Naturales y Agrobiologia, IRNAS-CSIC, 41012 Sevilla, Spain Departamento de Ciencias de la Tierra y del Medio Ambiente, Universidad de Alicante, 03080 Alicante, Spain Departamento de Biologia y Geologia, Universidad de Almeria, 04120 Almeria, Spain; acortes@ual.es Departamento de Geologia, Geograﬁa y Medio Ambiente, Universidad de Alcala, 28802 Alcala de Henares, Spain; soledad.cuezva@uah.es * Correspondence: saiz@irnase.csic.es † These authors contributed equally to this work. Abstract: The genus Crossiella contains two species, C. equi, causing nocardioform placentitis in horses, and C. cryophila, an environmental bacterium. Apart from C. equi, which is not discussed here, environmental Crossiella is rarely reported in the literature; thus, it has not been included among “rare actinobacteria”, whose isolation frequency is very low. After C. cryophila, only ﬁve reports cover the isolation of Crossiella strains. However, the frequency of published papers on environmental Crossiella has increased signiﬁcantly in recent years due to the extensive use of next-generation sequencing (NGS) and a huge cascade of data that has improved our understanding of how bacteria occur in the environment. In the last ﬁve years, Crossiella has been found in different environments (caves, soils, plant rhizospheres, building stones, etc.). The high abundance of Crossiella in cave moonmilk indicates that this genus may have an active role in moonmilk formation, as evidenced by the precipitation Citation: Martin-Pozas, T.; of calcite, witherite, and struvite in different culture media. This review provides an overview of Gonzalez-Pimentel, J.L.; Jurado, V.; environmental Crossiella, particularly in caves, and discusses its role in biomineralization processes Laiz, L.; Cañaveras, J.C.; Fernandez-Cortes, A.; Cuezva, S.; and bioactive compound production. Sanchez-Moral, S.; Saiz-Jimenez, C. Crossiella, a Rare Actinomycetota Keywords: Crossiella; biofilms; caves; moonmilk; biomineralization; rhizosphere; soils; bioactive compounds Genus, Abundant in the Environment. Appl. Biosci. 2023, 2, 194–210. https://doi.org/10.3390/ applbiosci2020014 1. Introduction Academic Editor: Robert Henry The ﬁrst strain included in the genus Crossiella has a long history of transfers and amendments. Takahashi et al. [1] studied the soil isolate Nocardiopsis mutabilis, capable of Received: 4 March 2023 producing novel antibiotics, and classiﬁed it as a new subspecies: Nocardiopsis mutabilis Revised: 24 April 2023 subsp. Cryophilis based on its growth at low temperatures (8–33 C). This strain was Accepted: 27 April 2023 subsequently transferred by Labeda and Lechevalier [2] to the genus Saccharothrix as Published: 6 May 2023 Saccharothrix cryophilis because its morphological and chemotaxonomical properties were more typical of the genus Saccharothrix than Nocardiopsis. In another study, Labeda [3] erected the genus Crossiella to accommodate the species Saccharothrix cryophilis, which was Copyright: © 2023 by the authors. misplaced within the genus Saccharothrix. The genus only contained the species Crossiella Licensee MDPI, Basel, Switzerland. cryophila, which was soon accompanied by Crossiella equi, responsible for causing abortion This article is an open access article cases in horses with equine nocardioform placentitis in Kentucky [4]. distributed under the terms and In the last 20 years, no other species of Crossiella have been described, with scarce conditions of the Creative Commons reports on the isolation of Crossiella strains in the literature. Sánchez-Moral [5] isolated a Attribution (CC BY) license (https:// few strains of Crossiella from Altamira Cave, Spain. Adeyemo and Onilude [6] described creativecommons.org/licenses/by/ a strain of Crossiella isolated from Nigerian soil with a broad spectrum of antimicrobial 4.0/). Appl. Biosci. 2023, 2, 194–210. https://doi.org/10.3390/applbiosci2020014 https://www.mdpi.com/journal/applbiosci Appl. Biosci. 2023, 2 195 activity. Cimermanova et al. [7] isolated nine actinobacteria collected from different heavy metal-contaminated soils and found that one strain could represent a new species within the genus Crossiella; however, they did not provide any characterization or description other than its position in the phylogenetic tree and that the strain differed from Crossiella cryophila in several biochemical properties. González-Riancho [8] isolated three Crossiella strains from white and grey bioﬁlms from Altamira Cave. Finally, Gonzalez-Pimentel et al. [9] studied the genomes of two Crossiella strains selected from 13 strains previously isolated from Altamira Cave (unpublished report). The isolation of Crossiella strains on only ﬁve occasions in the last 10 years included this genus within the so-called “rare actinobacteria”. Oren and Garrity [10] considered Acti- nobacteria a synonym of Actinomycetota. They presented the names and formal descriptions of 42 phyla to effect valid publication in their names based on genera as nomenclatural types. However, in this paper, we maintained the original names, as previously published by each author, to avoid mistakes. “Rare actinobacteria” are non-Streptomyces actinobacteria whose isolation frequency is much lower than Streptomyces strains, commonly isolated by conventional methods [11,12]. Tiwari and Gupta [13,14] reported 120 new genera of “rare actinobacteria” in the ﬁrst decade of the 21st century. A total of 40 out of 120 genera were isolated from soils with com- paratively lower percentages from other environments: marine and freshwater sediments, marine animals, plants, buildings, etc. A few reports included the rare genera Actinomadura, Nonomuraea, Micromonospora, Streptosporangium, Nocardiopsis, and Pseudonocardia as most frequent in diverse environments [15–20]. It is noteworthy that an abundance of “rare actinobacteria” is in extreme environments, as exempliﬁed in Atacama [18] and other deserts [21–24]. However, Crossiella has not been included among “rare actinobacteria” thus far. We have found that Crossiella is an abundant genus in most studied Spanish caves, whether they are gypsum, karstic, or volcanic [9,25–27], and in other terrestrial and aquatic environments. In this paper, we review the occurrence of environmental Crossiella, its relative abun- dance in Spanish caves and other subterranean environments, as well as its involvement in caves’ mineral precipitation. The interest in Crossiella lies in its role in biomineralization and potential use in biotechnological processes (stone bioconsolidation, enzyme sources, bioactive compounds, etc.). 2. The Genus Crossiella in Caves Table 1 shows the occurrence of Crossiella in different Spanish caves. The high relative abundance of this genus is in moonmilk (Figure 1), either from karstic (Pindal) or volcanic (Fuente de la Canaria and Bucara II) caves, as well as in coloured bioﬁlms (Pindal, Altamira, Castañar, Covadura) is remarkable [27–31]. The relative humidity is near 100% in these caves. In addition, other mineral/biological formations, such as a pink formation in Bucara II, exhibit high relative abundance (38.9%). Similarly, formations such as mucous formations or brown deposits also reach relatively high abundances (6.7–12.8%) [29]. Interestingly, low percentages of Crossiella found in the sediments under the moonmilk indicate an aerobic behaviour for this genus [3]. Crossiella was also found in phototrophic bioﬁlms from Nerja Cave [30]. Table 1. Occurrence and relative abundance (>1%) of Crossiella in Spanish karstic environments, as reported in NGS studies. Cave Relative Abundance Genus Type of Sample References 16.0–27.1 Crossiella Moonmilk 1.4–1.7 Crossiella Sediment under moonmilk [26,28,31] Pindal 11.3–11.7 Crossiella Top-layer sediments Appl. Biosci. 2023, 2 196 Table 1. Cont. Cave Relative Abundance Genus Type of Sample References 6.0–9.0 Crossiella Sediments 5.3–7.9 Crossiella Yellow bioﬁlm 2.0–8.0 Crossiella Grey bioﬁlms 7.0–8.0 Crossiella Pink bioﬁlms 12.6–12.8 Crossiella Mucous formations 12.3 Crossiella Moonmilk [29] Fuente de la Canaria 6.7 Crossiella Brown and yellow deposits 38.9 Crossiella Pink deposit Bucara II [29] 24.9 Crossiella Moonmilk Nerja 0.1–1.5 Crossiella Phototrophic bioﬁlms [30] Castañar 15.0 Crossiella Grey bioﬁlm [31] >20.0 Crossiella Grey bioﬁlms Altamira 27.0 Crossiella White bioﬁlms [30] 38.0 Crossiella Yellow bioﬁlms 26.4–54.1 Crossiella White bioﬁlm Covadura 21.8–51.9 Crossiella Yellow bioﬁlm Unpublished data 4.5–19.7 Crossiella Sediments Yeso 1.3–13.3 Crossiella Sediments Unpublished data 16.6 Crossiella White bioﬁlm Thyssen Museum 64.2 Crossiella Grey bioﬁlm [32] basement Appl. Biosci. 2023, 2, FOR PEER REVIEW 4 2.8–7.4 Crossiella Sediment Figure 1. Scanning electron micrographs of moonmilk deposits in Pindal Cave, Spain. (a) Longitu- Figure 1. Scanning electron micrographs of moonmilk deposits in Pindal Cave, Spain. (a) Lon- dinal view of sediment covered by moonmilk. (b,c) Crystalline calcite fibres (red arrow) and Acti- gitudinal view of sediment covered by moonmilk. (b,c) Crystalline calcite ﬁbres (red arrow) and nomycetota filaments (blue arrow). (d) Scanning electron micrographs and EDX spectra of crystal- Actinomycetota ﬁlaments (blue arrow). (d) Scanning electron micrographs and EDX spectra of crys- line calcite fibres . Note the swelling of filaments in (c), similar to those reported for Crossiella cry- ophila [3]. talline calcite ﬁbres. Note the swelling of ﬁlaments in (c), similar to those reported for Crossiella cryophila [3]. Table 2 shows the widespread occurrence of Crossiella in caves in the USA, France and China. Less frequent records were found in caves in Italy, Pakistan, Portugal, Serbia, and Thailand, among other countries [35–57]. Table 2. Occurrence and relative abundance (>1%) of Crossiella in caves all over the world. Relative Karstic Caves Genus Type of Sample (Method) References Abundance% Heshang n.d. Crossiella Weathered rocks (NGS) [35] Laugerie-Haute 4.0 Crossiella Salt efflorescences (clones) [36] Sorcerers 30.0 Crossiella Salt efflorescences (NGS) [37] Pillier n.d. Crossiella Wall rock (NGS) [38] Yixing Shanjuan 3.9 Crossiella Speleothem (NGS) [39] Shuanghe 9.5 Crossiella Rock (NGS) [40] Manao-Pee 4.1 Crossiella Soil (NGS) [41] KN14 27.1–52.3 Crossiella Rock/Clay (NGS) [42] RN5 1.0–17.9 Crossiella Rock/Clay/Mud (NGS) [42] Maijishan Grottoes n.d. Crossiella Walls paintings (NGS) [43] Heshang n.d. Crossiella Weathered rocks (NGS) [44] Kashmir and Tiser 11.9–36.6 Crossiella Soil (NGS) [45] Zhijin 4.1 Crossiella Wall rock (NGS) [46] Rouffignac ~70.0 Crossiella Wall rock (NGS) [47] Stiffe 9.9 Crossiella Biofilms (NGS) [48] Heshang n.d. Crossiella Weathered rocks (NGS) [49] Appl. Biosci. 2023, 2 197 Crossiella, at a relative abundance of 15.0%, was found in grey bioﬁlms from Castañar Cave [31]. Similar grey bioﬁlms were observed in Altamira Cave [8] and the Thyssen Museum, reaching a relative abundance of 64.2% [32]. Data from a geomicrobiological study of a Roman nymphaeum located in the archaeological basement of the Thyssen Museum in Malaga, Spain, were also included in Table 1 due to its interest. The environmental conditions of this archaeological basement are special because they mix the characteristics of an environment heavily inﬂuenced by the natural underlying karst system with those of an enclosure located in an urban building. Apart from caves, it was remarkable that a subterranean environment, the Roman mortar pavement in the archaeological basement, was colonized by grey bioﬁlms with a high relative abundance of Crossiella. This environment is characterized by permanent darkness, the absence of visits, and high relative humidity. Table 1 shows the occurrence of Crossiella in moonmilk, grey, yellow, pink and white bioﬁlms, and sediments from different caves and subterranean environments. Crossiella is abundant in different types of rocks, either in volcanic (Fuente de la Canaria, Bucara II), karstic (Pindal, Nerja, Castañar, Altamira) or gypsum (Covadura, Yeso) caves. In addition to the studies in Table 1, authors have reported the occurrence of Crossiella using methodological approaches other than NGS. Stomeo et al. [33] found metaboli- cally active Crossiella in white bioﬁlms from Ardales Cave, Malaga, Spain. Portillo and Gonzalez [34] identiﬁed Crossiella as a major metabolically active bacterium in the black crust of a shelter located in Aragon, Spain, and Sanchez-Moral [5] reported Crossiella in Altamira Cave. Table 2 shows the widespread occurrence of Crossiella in caves in the USA, France and China. Less frequent records were found in caves in Italy, Pakistan, Portugal, Serbia, and Thailand, among other countries [35–57]. Table 2. Occurrence and relative abundance (>1%) of Crossiella in caves all over the world. Relative Karstic Caves Genus Type of Sample (Method) References Abundance% Heshang n.d. Crossiella Weathered rocks (NGS) [35] Laugerie-Haute 4.0 Crossiella Salt efﬂorescences (clones) [36] Sorcerers 30.0 Crossiella Salt efﬂorescences (NGS) [37] Pillier n.d. Crossiella Wall rock (NGS) [38] Yixing Shanjuan 3.9 Crossiella Speleothem (NGS) [39] Shuanghe 9.5 Crossiella Rock (NGS) [40] Manao-Pee 4.1 Crossiella Soil (NGS) [41] KN14 27.1–52.3 Crossiella Rock/Clay (NGS) [42] RN5 1.0–17.9 Crossiella Rock/Clay/Mud (NGS) [42] Maijishan Grottoes n.d. Crossiella Walls paintings (NGS) [43] Heshang n.d. Crossiella Weathered rocks (NGS) [44] Kashmir and Tiser 11.9–36.6 Crossiella Soil (NGS) [45] Zhijin 4.1 Crossiella Wall rock (NGS) [46] Roufﬁgnac ~70.0 Crossiella Wall rock (NGS) [47] Stiffe 9.9 Crossiella Bioﬁlms (NGS) [48] Heshang n.d. Crossiella Weathered rocks (NGS) [49] Cave Church 0.1–4.9 Crossiella Fresco (NGS) [50] Volcanic Caves Azorean caves 18.6 Crossiella Bioﬁlms (clones) [51] Appl. Biosci. 2023, 2 198 Table 2. Cont. Relative Karstic Caves Genus Type of Sample (Method) References Abundance% Hawaiian caves n.d. Crossiella Bioﬁlms (NGS) [52] Californian caves n.d. Crossiella Bioﬁlms (NGS) [53] Idahoan caves n.d. Crossiella Bioﬁlms (NGS) [54] Sicilian caves 62.5–77.6 Crossiella Bioﬁlms (NGS) [55] Other Cave Types Carlsbad Cavern n.d. Crossiella Rocks (clones) [56] Imawarì Yeuta n.d. Crossiella Patina/Speleothems (NGS) [57] n.d. Not determined. Apart from the high abundance in Spanish caves, the high relative abundance of Crossiella in Italian caves is also remarkable. In this regard, Nicolosi et al. [55] recorded high relative abundances in four Etna volcano caves. One of them ranged from 62.5 to 77.6%. Other notable abundances were found in the salt efﬂorescences of a French shelter [37] and in caves in the USA [42], France [47], Pakistan [45], and the Azores, Portugal [51]. Crossiella has been identiﬁed as one of the dominant bacterial phylotypes, with an in- creasing prevalence when global humidity conditions rise, in a research covering 1050 cave microbiomes worldwide (manuscript in preparation). 3. Crossiella in the Environment Supplementary Table S1 lists papers in the literature that use the keyword “Crossiella”, including Crossiella misspelling [58–146]. The occurrence of the genus Crossiella in different environments is signiﬁcant. Papers reporting Crossiella equi and its involvement in animal diseases [4] were excluded. The papers listed in Supplementary Table S1 rely on molecular methods, except for ﬁve articles describing the properties of isolated strains [5–9]. The genus Crossiella shows a ubiquitous and extensive geographical distribution on all continents, including Antarctica, but not in Australia/Oceania, likely due to a lack of relevant studies. Fewer reports locate Crossiella in mines and reclaimed mine soils [7,120–124]. How- ever, the number of studies on its presence in soils and the rhizospheres of diverse plants is considerable. Several Crossiella ﬁndings in stones and building stones were also conﬁrmed [125–138]. Finally, a few records in sea sediments and freshwaters were signiﬁcant [139–146] because they included aquatic environments among Crossiella habitats. From Supplementary Table S1, we can conclude that Crossiella, in addition to caves, is relatively abundant in diverse environments, namely soils, plant rhizospheres, mines, building stones, and other occasional habitats, but is rarely isolated. Considering the abundance of reports on Crossiella in soils [58–96] and plant rhizo- spheres [97–119], the presence of this genus in caves and other subterranean environments could be attributed to its transport to the subsurface via percolation waters. In this regard, Crossiella in percentages <1% have been found in drip waters from Pindal Cave [28]. It may be possible that once transported to the caves, the environmental conditions favour and increase the colonization and growth of Crossiella on different mineral substrata. 4. Crossiella Isolates Only ﬁve reports shed light on Crossiella isolates. A screening of Nigerian soils resulted in the isolation of Crossiella sp. strain EK18. The 16S rRNA nucleotide sequence showed 98% similarity to C. equi. This strain grew well in different culture media and exhibited broad-spectrum antimicrobial activity [6]. The authors studied the effects of pH, temperature, carbon and nitrogen sources, sodium chloride concentration, and incubation time on antimicrobial activity. In addition, they reported a list of 12 so-called antimicrobial Appl. Biosci. 2023, 2 199 metabolites, including alkanes, alkenes, commonly synthesized by bacteria, and phthalates, which are contaminants from materials and impurities from products used in culture media. Therefore, no conclusive data on the real bioactive compounds produced by the Crossiella strain can be derived from this study. Cimermanova et al. [7] isolated Crossiella sp., strain S2, from mining wastes, with a 16rRNA gene sequence similarity of 99.1% to C. cryophila. The authors suggested that it may represent a novel, never described species, based on its location in the phylogenetic tree. The strain also exhibited high heavy metal resistance. González-Riancho [8] found relative abundances of Crossiella >20% in white, yellow, and grey bioﬁlms from Altamira Cave. She isolated two strains from white and one strain from grey bioﬁlms with similarities of 99.0–100.0 to C. cryophila using the medium Actinomycete Isolation Agar (AIA). Gonzalez-Pimentel et al. [9] studied two of the thirteen Crossiella strains previously isolated from grey bioﬁlms colonizing Altamira Cave, Spain (unpublished report). In vitro and in silico analyses showed the inhibition of pathogenic bacteria and fungi. The exclusive combination of gene clusters involved in the synthesis of lanthipeptides, lasso peptides, nonribosomal peptides and polyketides indicates that these two strains represent a source of new bioactive compounds. The taxonomical distance of both strains from their closest relative, C. cryophila, suggests that they represent a new species of Crossiella, which will be described in future works. So far, the low number of isolated Crossiella strains indicates that most of the culture media used are inadequate to reproduce their growth in the laboratory. The environmental conditions of their ecological niche should also be considered when designing speciﬁc culture media, which are superior to conventional ones. 5. Biomineralization in Caves Induced by Crossiella Biomineralization or crystal formation is a general phenomenon caused by soil bacteria, as reported by Boquet et al. [147]. These authors isolated 210 bacteria that could form calcite crystals in a medium with calcium acetate and stated that their occurrence depended on the composition of the medium used. The role of bacteria in speleogenesis has been discussed for decades. Barton and Northup [148] stated that in the 1960s, a few authors proposed that microbes played a role in forming cave deposits. Banks et al. [149] conﬁrmed the link between calcium metabolism 2+ in bacteria and calciﬁcation using cave isolates. They suggested that the toxicity of Ca 2+ ions to bacteria promoted the need to remove Ca ions from the cell via calciﬁcation as a detoxiﬁcation mechanism. Further evidence of biomineralization has been reported in recent decades that sheds light on microbially induced mineral precipitation [150–153]. This precipitation has been attributed to several causes: the modulation of environmental pH, nucleation sites on cell surfaces, or enzymatically driven processes involving carbonic anhydrase, urease, etc. [154]. Grey bioﬁlms from Altamira Cave were studied, and scanning electron microscopy (SEM) revealed an abundance of bioinduced calcite crystals in addition to moonmilk [152]. The bioﬁlms mainly comprised Actinomycetota ﬁlaments promoting carbon dioxide uptake and formation of calcite deposits. A model for bioinduced calcite formation, supported by scanning and transmission electron microscopy data, was proposed by Cuezva et al. [152]. Apart from the precipitation of calcite by Crossiella, another experiment (Figure 2) with two strains of Crossiella isolated from Altamira Cave [9] revealed that both strains induced the formation of different crystals when incubated in a culture medium with barium acetate, yeast extract, and agar (Ba1). Two crystal types were identiﬁed on the plates: witherite (barium carbonate) and struvite (magnesium ammonium phosphate), with distinct abundances that were higher for witherite and scarcer for struvite. Witherite precipitation is due to an abundance of barium in the medium. Occasional struvite crystals can be derived from the amino acids and minor amounts of phosphorus and magnesium in the yeast extract [155]. Appl. Biosci. 2023, 2, FOR PEER REVIEW 7 Appl. Biosci. 2023, 2 200 tals can be derived from the amino acids and minor amounts of phosphorus and magne- sium in the yeast extract [155]. Figure 2. Scanning electron micrographs and EDX spectra of barium carbonate and phosphate Figure 2. Scanning electron micrographs and EDX spectra of barium carbonate and phosphate crystals from two strains of Crossiella sp. (Cross-1 and Cross-2) [7]. (a) Witherite (barium carbonate) crystals from two strains of Crossiella sp. (Cross-1 and Cross-2) [7]. (a) Witherite (barium carbonate) crystals and Crossiella filaments in culture medium Ba1 (Cross -1). (b) Witherite crystals in culture m crystals edium and Ba1 Cr (Cr ossiella oss-2).ﬁlaments (c) Struvite in (mag cultur nesi e me um dium amm Ba1 oniu (Cr m oss-1). phosph(ate) b) W crystal itherits ein crystals culture in mcultur edium e medium Ba1 (Cross-2). (c) Struvite (magnesium ammonium phosphate) crystals in culture medium Ba1 (Cross-1). (d) Crossiella ﬁlaments without crystal formation in tryptic soy agar medium (Cross-2). Appl. Biosci. 2023, 2 201 Baryte (barium sulphate) precipitation by bacteria was previously reported by Joubert et al. [156]. Sanchez-Moral et al. [157] found that baryte was associated with ﬁlamentous bacteria in altered volcanic rocks. Agromyces spp., Bacillus spp., Lysobacter spp., Ralstonia sp., Stenotrophomonas maltophilia, and Streptomyces sp. were isolated from the volcanic rocks and precipitated witherite or calcite/vaterite in media with barium or calcium acetate, respectively. The occurrence of baryte, but not witherite, in volcanic rocks was due to the presence of sulphate ions that easily transform witherite into barite. This transformation was not produced on the Crossiella plates without sulphate ions. Struvite precipitation is not as widespread as calcite or witherite in bacteria. Sanchez- Moral et al. [158] tested eight bacteria isolated from the Roman catacombs of St. Callixtus and Domitilla and reported that Agromyces ramosus precipitated calcite, magnesium calcite, witherite, and struvite, depending on the media composition. Other bacteria precipitating struvite were Bacillus sp. and Ralstonia metallidurans. Rivadeneyra et al. [159] found that only 20.8% of the tested bacterial isolates pre- cipitated struvite and that calcium acetate appeared to inhibit struvite precipitation in culture media, whereas ammonium ions triggered it [160]. Manzoor et al. [161] stated that urease-producing bacteria play a key role in struvite precipitation, controlling nucleation, and modulating crystalline phases and crystal shapes. Urease is present in the strain type of Crossiella, C. cryophila [3], and urease genes have been identiﬁed in the genomes of the two Crossiella strains from Altamira Cave [9]. Sánchez-Román et al. [162] reported that carbon and phosphorus cycles are interrelated during biomineralization. They also demonstrated the co-precipitation of carbonate and struvite, which we also found in Crossiella strains. The data reported show that biomineralization by Crossiella is an active process in the presence of different ions, conﬁrming its role in moonmilk formation. Crossiella strains’ ability to induce carbonate precipitation, which is used to consolidate cultural heritage stones and buildings, should be explored. 6. Moonmilk Formation Moonmilk formation has been discussed in the literature for a long time [150,163–168]. The question: Is moonmilk an abiotic process driven physicochemically, or is it biotic, mediated by microorganisms? A biological origin currently prevails; even a combination of physicochemical and biogenic processes is being considered [166]. Cañaveras et al. [150,165] indicated that bacteria inﬂuenced the physicochemistry of calcite precipitation. They ob- served that cave moonmilk comprises a network of calcite crystals and active ﬁlamentous bacteria. They also found that hydromagnesite and needle-ﬁbre aragonite deposits were associated with bacteria in Altamira Cave, predominantly Streptomyces, for which they demonstrated their ability to precipitate calcite/vaterite in the laboratory. The association between bacteria and mineral crystals was reported in other papers and described using SEM [152,153,165,168–170]. In addition, different bacterial genera such as Agromyces, Amy- colatopsis, Brachybacterium, Nocardioides, Nocardiopsis, Paenibacillus, and Rothia precipitated vaterite/calcite and Mg-calcite [171]. Maciejewska et al. [153] found that all the Streptomyces strains tested could promote calciﬁcation and biomineralization. The metabolic activities involved in the precipita- tion were amino acids ammoniﬁcation and ureolysis, which increased environmental pH. Sanchez-Moral et al. [169] stated that microbial activity induces carbonate precipitation in the early stages of deposition. However, as carbonate accumulates, a progressive decline in microbial activity occurs, as deduced from the RNA/DNA ratio, which is used as a marker of metabolic activity. The decreased metabolic activity is due to the progressive accumulation of carbonate and bacterial entrapment in mineral deposits. The high relative abundance of Crossiella in moonmilk from different caves indicates that this genus is active in moonmilk formation (Table 1). Enzymatic processes induce this mineralization, and several enzymes have been linked to Crossiella activity in moon- milk. Martin-Pozas et al. [26] suggested that moonmilk formation is related to syntrophic Appl. Biosci. 2023, 2 202 relationships between Crossiella and nitrifying bacteria, and Cuezva et al. [27] associated Crossiella with the ability to capture CO from the atmosphere and precipitate calcium carbonate as a by-product of carbonic anhydrase action, as observed in cave moonmilk. 7. Is Moonmilk a Source of Bioactive Compounds? Caves and moonmilk are colonized by complex bacterial communities. Maciejewska et al. [153] reported that Proteobacteria was the dominant phylum of moonmilk from a Belgian cave, followed by Actinobacteria, Acidobacteria, Chloroﬂexi, Nitrospirae, Gem- matimonadetes, and Planctomycetes. These seven phyla accounted for 85.8–90.2% of the total community. Martin-Pozas et al. [26] investigated the moonmilk composition from Pindal Cave in Spain. They found that Proteobacteria and Actinobacteria dominated the community with over 30% of relative abundance for each phyla, followed by Acidobacteria, Chloroﬂexi, Planctomycetes, Gemmatimonadetes, and Nitrospirae. These phyla accounted for 93.1–93.9% of the total community. The similarities between the phyla compositions of moonmilk from two different caves are remarkable. Moonmilk from a geographically distant cave [172] and another subterranean environment [173] also showed relatively similar phyla compositions. Moonmilk has been a promising reservoir for novel bacteria producing bioactive compounds, and a few novel species have been isolated, namely Streptomyces lunaelac- tis [174], Pseudomonas karstica, and Pseudomonas spelaei [175]. Several studies have stressed the great diversity of unknown bacteria inhabiting moonmilk and the isolates’ production of bioactive compounds [176–178]. The high abundance of Actinomycetota (=Actinobacteria) and Pseudomonadota (=Pro- teobacteria) in moonmilk has prompted researchers to test a series of strategies to isolate hard-to-culture “rare actinobacteria” and discover novel bioactive compounds [13,14]. Adam et al. [176] obtained 40 isolates represented by Agromyces, Amycolatopsis, Kocuria, Micrococcus, Micromonospora, Nocardia, Streptomyces, and Rhodococcus species. The Strep- tomyces isolates displayed strong inhibitory activities against Gram-positive and Gram- negative bacteria and fungi [179]. Genome mining of Streptomyces lunaelactis revealed 42 biosynthetic gene clusters [180] and the production of the antibiotics bagremycins and lunaemycins [180,181]. The genome of Crossiella, abundant in moonmilk [26], showed the presence of a combination of gene clusters involved in synthesising different bioactive com- pounds [9]. The data suggest the possibility of ﬁnding other moonmilk bacteria involved in synthesising bioactive compounds. 8. Conclusions The genus Crossiella is widely distributed in all environments, reaching a relative abundance of up to 78% in a Sicilian cave. Its occurrence in soils, plant rhizospheres and caves is especially important. The last case is probably due to its transport to the subsurface by percolating waters. Despite this abundance, the strains isolated were scarce. The data suggest that more environmental Crossiella species are waiting to be described, apart from Crossiella cryophila and Crossiella equi. The increasing number of metagenomic sequence data from all environments offers clear opportunities to guide the isolation and cultivation of Crossiella. Therefore, further efforts are required to design suitable isolation culture media. They should consider the environmental conditions of the niches where Crossiella thrives, namely alkaline pH and high mineral concentrations. Crossiella has an important role in carbon sequestration in subterranean environments. Metagenomic studies and isolating more Crossiella strains and/or species are the only way to advance knowledge of Crossiella functions in different ecosystems. Furthermore, its role in biomineralization and moonmilk formation is also apparent. Finally, Crossiella appears to be a promising source of active compounds, and the isolated strains deserve more attention regarding their potential use in biotechnological processes. Appl. Biosci. 2023, 2 203 Supplementary Materials: The following supporting information can be downloaded at: https:// www.mdpi.com/article/10.3390/applbiosci2020014/s1, Table S1: Occurrence of the genus Crossiella in different environments. Author Contributions: Conceptualization, C.S.-J. and S.S.-M.; investigation, T.M.-P., J.L.G.-P., V.J., L.L., J.C.C., A.F.-C. and S.C.; writing—original draft preparation, C.S.-J., S.S.-M. and T.M.-P.; writing— review and editing, C.S.-J. and S.S.-M. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the projects PID2020-114978GB-I00 and PID2019-110603RB-I00. The Malaga City Council ﬁnanced data from the archaeological basement of the Thyssen Museum of Malaga through a conservation contract for this Roman site. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: All data reported in this review can be found in the relevant papers cited. Scanning electron micrographs, EDX spectra, and unpublished data are available on request from Sergio Sanchez-Moral. Acknowledgments: This is a contribution from CSIC Interdisciplinary Thematic Platform Open Heritage: Research and Society (PTI-PAIS). Conﬂicts of Interest: The authors declare no conﬂict of interest. References 1. Takahashi, A.; Hotta, K.; Saito, N.; Morioka, M.; Okami, Y.; Umezawa, H. Production of novel antibiotic, dopsisamine, by a new subspecies of Nocardiopsis mutabilis with multiple antibiotic resistance. J. Antibiot. 1986, 39, 175–183. [CrossRef] [PubMed] 2. Labeda, D.P.; Lechevalier, M.P. 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Abstract

Review Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment 1 , † 2 , † 3 3 4 Tamara Martin-Pozas , Jose Luis Gonzalez-Pimentel , Valme Jurado , Leonila Laiz , Juan Carlos Cañaveras , 5 6 1 3 , Angel Fernandez-Cortes , Soledad Cuezva , Sergio Sanchez-Moral and Cesareo Saiz-Jimenez * Museo Nacional de Ciencias Naturales, MNCN-CSIC, 28006 Madrid, Spain Centro Andaluz de Biologia del Desarrollo (CABD, UPO-CSIC-JA), Facultad de Ciencias Experimentales, Departamento de Genetica, Universidad Pablo de Olavide, 41013 Sevilla, Spain Instituto de Recursos Naturales y Agrobiologia, IRNAS-CSIC, 41012 Sevilla, Spain Departamento de Ciencias de la Tierra y del Medio Ambiente, Universidad de Alicante, 03080 Alicante, Spain Departamento de Biologia y Geologia, Universidad de Almeria, 04120 Almeria, Spain; acortes@ual.es Departamento de Geologia, Geograﬁa y Medio Ambiente, Universidad de Alcala, 28802 Alcala de Henares, Spain; soledad.cuezva@uah.es * Correspondence: saiz@irnase.csic.es † These authors contributed equally to this work. Abstract: The genus Crossiella contains two species, C. equi, causing nocardioform placentitis in horses, and C. cryophila, an environmental bacterium. Apart from C. equi, which is not discussed here, environmental Crossiella is rarely reported in the literature; thus, it has not been included among “rare actinobacteria”, whose isolation frequency is very low. After C. cryophila, only ﬁve reports cover the isolation of Crossiella strains. However, the frequency of published papers on environmental Crossiella has increased signiﬁcantly in recent years due to the extensive use of next-generation sequencing (NGS) and a huge cascade of data that has improved our understanding of how bacteria occur in the environment. In the last ﬁve years, Crossiella has been found in different environments (caves, soils, plant rhizospheres, building stones, etc.). The high abundance of Crossiella in cave moonmilk indicates that this genus may have an active role in moonmilk formation, as evidenced by the precipitation Citation: Martin-Pozas, T.; of calcite, witherite, and struvite in different culture media. This review provides an overview of Gonzalez-Pimentel, J.L.; Jurado, V.; environmental Crossiella, particularly in caves, and discusses its role in biomineralization processes Laiz, L.; Cañaveras, J.C.; Fernandez-Cortes, A.; Cuezva, S.; and bioactive compound production. Sanchez-Moral, S.; Saiz-Jimenez, C. Crossiella, a Rare Actinomycetota Keywords: Crossiella; biofilms; caves; moonmilk; biomineralization; rhizosphere; soils; bioactive compounds Genus, Abundant in the Environment. Appl. Biosci. 2023, 2, 194–210. https://doi.org/10.3390/ applbiosci2020014 1. Introduction Academic Editor: Robert Henry The ﬁrst strain included in the genus Crossiella has a long history of transfers and amendments. Takahashi et al. [1] studied the soil isolate Nocardiopsis mutabilis, capable of Received: 4 March 2023 producing novel antibiotics, and classiﬁed it as a new subspecies: Nocardiopsis mutabilis Revised: 24 April 2023 subsp. Cryophilis based on its growth at low temperatures (8–33 C). This strain was Accepted: 27 April 2023 subsequently transferred by Labeda and Lechevalier [2] to the genus Saccharothrix as Published: 6 May 2023 Saccharothrix cryophilis because its morphological and chemotaxonomical properties were more typical of the genus Saccharothrix than Nocardiopsis. In another study, Labeda [3] erected the genus Crossiella to accommodate the species Saccharothrix cryophilis, which was Copyright: © 2023 by the authors. misplaced within the genus Saccharothrix. The genus only contained the species Crossiella Licensee MDPI, Basel, Switzerland. cryophila, which was soon accompanied by Crossiella equi, responsible for causing abortion This article is an open access article cases in horses with equine nocardioform placentitis in Kentucky [4]. distributed under the terms and In the last 20 years, no other species of Crossiella have been described, with scarce conditions of the Creative Commons reports on the isolation of Crossiella strains in the literature. Sánchez-Moral [5] isolated a Attribution (CC BY) license (https:// few strains of Crossiella from Altamira Cave, Spain. Adeyemo and Onilude [6] described creativecommons.org/licenses/by/ a strain of Crossiella isolated from Nigerian soil with a broad spectrum of antimicrobial 4.0/). Appl. Biosci. 2023, 2, 194–210. https://doi.org/10.3390/applbiosci2020014 https://www.mdpi.com/journal/applbiosci Appl. Biosci. 2023, 2 195 activity. Cimermanova et al. [7] isolated nine actinobacteria collected from different heavy metal-contaminated soils and found that one strain could represent a new species within the genus Crossiella; however, they did not provide any characterization or description other than its position in the phylogenetic tree and that the strain differed from Crossiella cryophila in several biochemical properties. González-Riancho [8] isolated three Crossiella strains from white and grey bioﬁlms from Altamira Cave. Finally, Gonzalez-Pimentel et al. [9] studied the genomes of two Crossiella strains selected from 13 strains previously isolated from Altamira Cave (unpublished report). The isolation of Crossiella strains on only ﬁve occasions in the last 10 years included this genus within the so-called “rare actinobacteria”. Oren and Garrity [10] considered Acti- nobacteria a synonym of Actinomycetota. They presented the names and formal descriptions of 42 phyla to effect valid publication in their names based on genera as nomenclatural types. However, in this paper, we maintained the original names, as previously published by each author, to avoid mistakes. “Rare actinobacteria” are non-Streptomyces actinobacteria whose isolation frequency is much lower than Streptomyces strains, commonly isolated by conventional methods [11,12]. Tiwari and Gupta [13,14] reported 120 new genera of “rare actinobacteria” in the ﬁrst decade of the 21st century. A total of 40 out of 120 genera were isolated from soils with com- paratively lower percentages from other environments: marine and freshwater sediments, marine animals, plants, buildings, etc. A few reports included the rare genera Actinomadura, Nonomuraea, Micromonospora, Streptosporangium, Nocardiopsis, and Pseudonocardia as most frequent in diverse environments [15–20]. It is noteworthy that an abundance of “rare actinobacteria” is in extreme environments, as exempliﬁed in Atacama [18] and other deserts [21–24]. However, Crossiella has not been included among “rare actinobacteria” thus far. We have found that Crossiella is an abundant genus in most studied Spanish caves, whether they are gypsum, karstic, or volcanic [9,25–27], and in other terrestrial and aquatic environments. In this paper, we review the occurrence of environmental Crossiella, its relative abun- dance in Spanish caves and other subterranean environments, as well as its involvement in caves’ mineral precipitation. The interest in Crossiella lies in its role in biomineralization and potential use in biotechnological processes (stone bioconsolidation, enzyme sources, bioactive compounds, etc.). 2. The Genus Crossiella in Caves Table 1 shows the occurrence of Crossiella in different Spanish caves. The high relative abundance of this genus is in moonmilk (Figure 1), either from karstic (Pindal) or volcanic (Fuente de la Canaria and Bucara II) caves, as well as in coloured bioﬁlms (Pindal, Altamira, Castañar, Covadura) is remarkable [27–31]. The relative humidity is near 100% in these caves. In addition, other mineral/biological formations, such as a pink formation in Bucara II, exhibit high relative abundance (38.9%). Similarly, formations such as mucous formations or brown deposits also reach relatively high abundances (6.7–12.8%) [29]. Interestingly, low percentages of Crossiella found in the sediments under the moonmilk indicate an aerobic behaviour for this genus [3]. Crossiella was also found in phototrophic bioﬁlms from Nerja Cave [30]. Table 1. Occurrence and relative abundance (>1%) of Crossiella in Spanish karstic environments, as reported in NGS studies. Cave Relative Abundance Genus Type of Sample References 16.0–27.1 Crossiella Moonmilk 1.4–1.7 Crossiella Sediment under moonmilk [26,28,31] Pindal 11.3–11.7 Crossiella Top-layer sediments Appl. Biosci. 2023, 2 196 Table 1. Cont. Cave Relative Abundance Genus Type of Sample References 6.0–9.0 Crossiella Sediments 5.3–7.9 Crossiella Yellow bioﬁlm 2.0–8.0 Crossiella Grey bioﬁlms 7.0–8.0 Crossiella Pink bioﬁlms 12.6–12.8 Crossiella Mucous formations 12.3 Crossiella Moonmilk [29] Fuente de la Canaria 6.7 Crossiella Brown and yellow deposits 38.9 Crossiella Pink deposit Bucara II [29] 24.9 Crossiella Moonmilk Nerja 0.1–1.5 Crossiella Phototrophic bioﬁlms [30] Castañar 15.0 Crossiella Grey bioﬁlm [31] >20.0 Crossiella Grey bioﬁlms Altamira 27.0 Crossiella White bioﬁlms [30] 38.0 Crossiella Yellow bioﬁlms 26.4–54.1 Crossiella White bioﬁlm Covadura 21.8–51.9 Crossiella Yellow bioﬁlm Unpublished data 4.5–19.7 Crossiella Sediments Yeso 1.3–13.3 Crossiella Sediments Unpublished data 16.6 Crossiella White bioﬁlm Thyssen Museum 64.2 Crossiella Grey bioﬁlm [32] basement Appl. Biosci. 2023, 2, FOR PEER REVIEW 4 2.8–7.4 Crossiella Sediment Figure 1. Scanning electron micrographs of moonmilk deposits in Pindal Cave, Spain. (a) Longitu- Figure 1. Scanning electron micrographs of moonmilk deposits in Pindal Cave, Spain. (a) Lon- dinal view of sediment covered by moonmilk. (b,c) Crystalline calcite fibres (red arrow) and Acti- gitudinal view of sediment covered by moonmilk. (b,c) Crystalline calcite ﬁbres (red arrow) and nomycetota filaments (blue arrow). (d) Scanning electron micrographs and EDX spectra of crystal- Actinomycetota ﬁlaments (blue arrow). (d) Scanning electron micrographs and EDX spectra of crys- line calcite fibres . Note the swelling of filaments in (c), similar to those reported for Crossiella cry- ophila [3]. talline calcite ﬁbres. Note the swelling of ﬁlaments in (c), similar to those reported for Crossiella cryophila [3]. Table 2 shows the widespread occurrence of Crossiella in caves in the USA, France and China. Less frequent records were found in caves in Italy, Pakistan, Portugal, Serbia, and Thailand, among other countries [35–57]. Table 2. Occurrence and relative abundance (>1%) of Crossiella in caves all over the world. Relative Karstic Caves Genus Type of Sample (Method) References Abundance% Heshang n.d. Crossiella Weathered rocks (NGS) [35] Laugerie-Haute 4.0 Crossiella Salt efflorescences (clones) [36] Sorcerers 30.0 Crossiella Salt efflorescences (NGS) [37] Pillier n.d. Crossiella Wall rock (NGS) [38] Yixing Shanjuan 3.9 Crossiella Speleothem (NGS) [39] Shuanghe 9.5 Crossiella Rock (NGS) [40] Manao-Pee 4.1 Crossiella Soil (NGS) [41] KN14 27.1–52.3 Crossiella Rock/Clay (NGS) [42] RN5 1.0–17.9 Crossiella Rock/Clay/Mud (NGS) [42] Maijishan Grottoes n.d. Crossiella Walls paintings (NGS) [43] Heshang n.d. Crossiella Weathered rocks (NGS) [44] Kashmir and Tiser 11.9–36.6 Crossiella Soil (NGS) [45] Zhijin 4.1 Crossiella Wall rock (NGS) [46] Rouffignac ~70.0 Crossiella Wall rock (NGS) [47] Stiffe 9.9 Crossiella Biofilms (NGS) [48] Heshang n.d. Crossiella Weathered rocks (NGS) [49] Appl. Biosci. 2023, 2 197 Crossiella, at a relative abundance of 15.0%, was found in grey bioﬁlms from Castañar Cave [31]. Similar grey bioﬁlms were observed in Altamira Cave [8] and the Thyssen Museum, reaching a relative abundance of 64.2% [32]. Data from a geomicrobiological study of a Roman nymphaeum located in the archaeological basement of the Thyssen Museum in Malaga, Spain, were also included in Table 1 due to its interest. The environmental conditions of this archaeological basement are special because they mix the characteristics of an environment heavily inﬂuenced by the natural underlying karst system with those of an enclosure located in an urban building. Apart from caves, it was remarkable that a subterranean environment, the Roman mortar pavement in the archaeological basement, was colonized by grey bioﬁlms with a high relative abundance of Crossiella. This environment is characterized by permanent darkness, the absence of visits, and high relative humidity. Table 1 shows the occurrence of Crossiella in moonmilk, grey, yellow, pink and white bioﬁlms, and sediments from different caves and subterranean environments. Crossiella is abundant in different types of rocks, either in volcanic (Fuente de la Canaria, Bucara II), karstic (Pindal, Nerja, Castañar, Altamira) or gypsum (Covadura, Yeso) caves. In addition to the studies in Table 1, authors have reported the occurrence of Crossiella using methodological approaches other than NGS. Stomeo et al. [33] found metaboli- cally active Crossiella in white bioﬁlms from Ardales Cave, Malaga, Spain. Portillo and Gonzalez [34] identiﬁed Crossiella as a major metabolically active bacterium in the black crust of a shelter located in Aragon, Spain, and Sanchez-Moral [5] reported Crossiella in Altamira Cave. Table 2 shows the widespread occurrence of Crossiella in caves in the USA, France and China. Less frequent records were found in caves in Italy, Pakistan, Portugal, Serbia, and Thailand, among other countries [35–57]. Table 2. Occurrence and relative abundance (>1%) of Crossiella in caves all over the world. Relative Karstic Caves Genus Type of Sample (Method) References Abundance% Heshang n.d. Crossiella Weathered rocks (NGS) [35] Laugerie-Haute 4.0 Crossiella Salt efﬂorescences (clones) [36] Sorcerers 30.0 Crossiella Salt efﬂorescences (NGS) [37] Pillier n.d. Crossiella Wall rock (NGS) [38] Yixing Shanjuan 3.9 Crossiella Speleothem (NGS) [39] Shuanghe 9.5 Crossiella Rock (NGS) [40] Manao-Pee 4.1 Crossiella Soil (NGS) [41] KN14 27.1–52.3 Crossiella Rock/Clay (NGS) [42] RN5 1.0–17.9 Crossiella Rock/Clay/Mud (NGS) [42] Maijishan Grottoes n.d. Crossiella Walls paintings (NGS) [43] Heshang n.d. Crossiella Weathered rocks (NGS) [44] Kashmir and Tiser 11.9–36.6 Crossiella Soil (NGS) [45] Zhijin 4.1 Crossiella Wall rock (NGS) [46] Roufﬁgnac ~70.0 Crossiella Wall rock (NGS) [47] Stiffe 9.9 Crossiella Bioﬁlms (NGS) [48] Heshang n.d. Crossiella Weathered rocks (NGS) [49] Cave Church 0.1–4.9 Crossiella Fresco (NGS) [50] Volcanic Caves Azorean caves 18.6 Crossiella Bioﬁlms (clones) [51] Appl. Biosci. 2023, 2 198 Table 2. Cont. Relative Karstic Caves Genus Type of Sample (Method) References Abundance% Hawaiian caves n.d. Crossiella Bioﬁlms (NGS) [52] Californian caves n.d. Crossiella Bioﬁlms (NGS) [53] Idahoan caves n.d. Crossiella Bioﬁlms (NGS) [54] Sicilian caves 62.5–77.6 Crossiella Bioﬁlms (NGS) [55] Other Cave Types Carlsbad Cavern n.d. Crossiella Rocks (clones) [56] Imawarì Yeuta n.d. Crossiella Patina/Speleothems (NGS) [57] n.d. Not determined. Apart from the high abundance in Spanish caves, the high relative abundance of Crossiella in Italian caves is also remarkable. In this regard, Nicolosi et al. [55] recorded high relative abundances in four Etna volcano caves. One of them ranged from 62.5 to 77.6%. Other notable abundances were found in the salt efﬂorescences of a French shelter [37] and in caves in the USA [42], France [47], Pakistan [45], and the Azores, Portugal [51]. Crossiella has been identiﬁed as one of the dominant bacterial phylotypes, with an in- creasing prevalence when global humidity conditions rise, in a research covering 1050 cave microbiomes worldwide (manuscript in preparation). 3. Crossiella in the Environment Supplementary Table S1 lists papers in the literature that use the keyword “Crossiella”, including Crossiella misspelling [58–146]. The occurrence of the genus Crossiella in different environments is signiﬁcant. Papers reporting Crossiella equi and its involvement in animal diseases [4] were excluded. The papers listed in Supplementary Table S1 rely on molecular methods, except for ﬁve articles describing the properties of isolated strains [5–9]. The genus Crossiella shows a ubiquitous and extensive geographical distribution on all continents, including Antarctica, but not in Australia/Oceania, likely due to a lack of relevant studies. Fewer reports locate Crossiella in mines and reclaimed mine soils [7,120–124]. How- ever, the number of studies on its presence in soils and the rhizospheres of diverse plants is considerable. Several Crossiella ﬁndings in stones and building stones were also conﬁrmed [125–138]. Finally, a few records in sea sediments and freshwaters were signiﬁcant [139–146] because they included aquatic environments among Crossiella habitats. From Supplementary Table S1, we can conclude that Crossiella, in addition to caves, is relatively abundant in diverse environments, namely soils, plant rhizospheres, mines, building stones, and other occasional habitats, but is rarely isolated. Considering the abundance of reports on Crossiella in soils [58–96] and plant rhizo- spheres [97–119], the presence of this genus in caves and other subterranean environments could be attributed to its transport to the subsurface via percolation waters. In this regard, Crossiella in percentages <1% have been found in drip waters from Pindal Cave [28]. It may be possible that once transported to the caves, the environmental conditions favour and increase the colonization and growth of Crossiella on different mineral substrata. 4. Crossiella Isolates Only ﬁve reports shed light on Crossiella isolates. A screening of Nigerian soils resulted in the isolation of Crossiella sp. strain EK18. The 16S rRNA nucleotide sequence showed 98% similarity to C. equi. This strain grew well in different culture media and exhibited broad-spectrum antimicrobial activity [6]. The authors studied the effects of pH, temperature, carbon and nitrogen sources, sodium chloride concentration, and incubation time on antimicrobial activity. In addition, they reported a list of 12 so-called antimicrobial Appl. Biosci. 2023, 2 199 metabolites, including alkanes, alkenes, commonly synthesized by bacteria, and phthalates, which are contaminants from materials and impurities from products used in culture media. Therefore, no conclusive data on the real bioactive compounds produced by the Crossiella strain can be derived from this study. Cimermanova et al. [7] isolated Crossiella sp., strain S2, from mining wastes, with a 16rRNA gene sequence similarity of 99.1% to C. cryophila. The authors suggested that it may represent a novel, never described species, based on its location in the phylogenetic tree. The strain also exhibited high heavy metal resistance. González-Riancho [8] found relative abundances of Crossiella >20% in white, yellow, and grey bioﬁlms from Altamira Cave. She isolated two strains from white and one strain from grey bioﬁlms with similarities of 99.0–100.0 to C. cryophila using the medium Actinomycete Isolation Agar (AIA). Gonzalez-Pimentel et al. [9] studied two of the thirteen Crossiella strains previously isolated from grey bioﬁlms colonizing Altamira Cave, Spain (unpublished report). In vitro and in silico analyses showed the inhibition of pathogenic bacteria and fungi. The exclusive combination of gene clusters involved in the synthesis of lanthipeptides, lasso peptides, nonribosomal peptides and polyketides indicates that these two strains represent a source of new bioactive compounds. The taxonomical distance of both strains from their closest relative, C. cryophila, suggests that they represent a new species of Crossiella, which will be described in future works. So far, the low number of isolated Crossiella strains indicates that most of the culture media used are inadequate to reproduce their growth in the laboratory. The environmental conditions of their ecological niche should also be considered when designing speciﬁc culture media, which are superior to conventional ones. 5. Biomineralization in Caves Induced by Crossiella Biomineralization or crystal formation is a general phenomenon caused by soil bacteria, as reported by Boquet et al. [147]. These authors isolated 210 bacteria that could form calcite crystals in a medium with calcium acetate and stated that their occurrence depended on the composition of the medium used. The role of bacteria in speleogenesis has been discussed for decades. Barton and Northup [148] stated that in the 1960s, a few authors proposed that microbes played a role in forming cave deposits. Banks et al. [149] conﬁrmed the link between calcium metabolism 2+ in bacteria and calciﬁcation using cave isolates. They suggested that the toxicity of Ca 2+ ions to bacteria promoted the need to remove Ca ions from the cell via calciﬁcation as a detoxiﬁcation mechanism. Further evidence of biomineralization has been reported in recent decades that sheds light on microbially induced mineral precipitation [150–153]. This precipitation has been attributed to several causes: the modulation of environmental pH, nucleation sites on cell surfaces, or enzymatically driven processes involving carbonic anhydrase, urease, etc. [154]. Grey bioﬁlms from Altamira Cave were studied, and scanning electron microscopy (SEM) revealed an abundance of bioinduced calcite crystals in addition to moonmilk [152]. The bioﬁlms mainly comprised Actinomycetota ﬁlaments promoting carbon dioxide uptake and formation of calcite deposits. A model for bioinduced calcite formation, supported by scanning and transmission electron microscopy data, was proposed by Cuezva et al. [152]. Apart from the precipitation of calcite by Crossiella, another experiment (Figure 2) with two strains of Crossiella isolated from Altamira Cave [9] revealed that both strains induced the formation of different crystals when incubated in a culture medium with barium acetate, yeast extract, and agar (Ba1). Two crystal types were identiﬁed on the plates: witherite (barium carbonate) and struvite (magnesium ammonium phosphate), with distinct abundances that were higher for witherite and scarcer for struvite. Witherite precipitation is due to an abundance of barium in the medium. Occasional struvite crystals can be derived from the amino acids and minor amounts of phosphorus and magnesium in the yeast extract [155]. Appl. Biosci. 2023, 2, FOR PEER REVIEW 7 Appl. Biosci. 2023, 2 200 tals can be derived from the amino acids and minor amounts of phosphorus and magne- sium in the yeast extract [155]. Figure 2. Scanning electron micrographs and EDX spectra of barium carbonate and phosphate Figure 2. Scanning electron micrographs and EDX spectra of barium carbonate and phosphate crystals from two strains of Crossiella sp. (Cross-1 and Cross-2) [7]. (a) Witherite (barium carbonate) crystals from two strains of Crossiella sp. (Cross-1 and Cross-2) [7]. (a) Witherite (barium carbonate) crystals and Crossiella filaments in culture medium Ba1 (Cross -1). (b) Witherite crystals in culture m crystals edium and Ba1 Cr (Cr ossiella oss-2).ﬁlaments (c) Struvite in (mag cultur nesi e me um dium amm Ba1 oniu (Cr m oss-1). phosph(ate) b) W crystal itherits ein crystals culture in mcultur edium e medium Ba1 (Cross-2). (c) Struvite (magnesium ammonium phosphate) crystals in culture medium Ba1 (Cross-1). (d) Crossiella ﬁlaments without crystal formation in tryptic soy agar medium (Cross-2). Appl. Biosci. 2023, 2 201 Baryte (barium sulphate) precipitation by bacteria was previously reported by Joubert et al. [156]. Sanchez-Moral et al. [157] found that baryte was associated with ﬁlamentous bacteria in altered volcanic rocks. Agromyces spp., Bacillus spp., Lysobacter spp., Ralstonia sp., Stenotrophomonas maltophilia, and Streptomyces sp. were isolated from the volcanic rocks and precipitated witherite or calcite/vaterite in media with barium or calcium acetate, respectively. The occurrence of baryte, but not witherite, in volcanic rocks was due to the presence of sulphate ions that easily transform witherite into barite. This transformation was not produced on the Crossiella plates without sulphate ions. Struvite precipitation is not as widespread as calcite or witherite in bacteria. Sanchez- Moral et al. [158] tested eight bacteria isolated from the Roman catacombs of St. Callixtus and Domitilla and reported that Agromyces ramosus precipitated calcite, magnesium calcite, witherite, and struvite, depending on the media composition. Other bacteria precipitating struvite were Bacillus sp. and Ralstonia metallidurans. Rivadeneyra et al. [159] found that only 20.8% of the tested bacterial isolates pre- cipitated struvite and that calcium acetate appeared to inhibit struvite precipitation in culture media, whereas ammonium ions triggered it [160]. Manzoor et al. [161] stated that urease-producing bacteria play a key role in struvite precipitation, controlling nucleation, and modulating crystalline phases and crystal shapes. Urease is present in the strain type of Crossiella, C. cryophila [3], and urease genes have been identiﬁed in the genomes of the two Crossiella strains from Altamira Cave [9]. Sánchez-Román et al. [162] reported that carbon and phosphorus cycles are interrelated during biomineralization. They also demonstrated the co-precipitation of carbonate and struvite, which we also found in Crossiella strains. The data reported show that biomineralization by Crossiella is an active process in the presence of different ions, conﬁrming its role in moonmilk formation. Crossiella strains’ ability to induce carbonate precipitation, which is used to consolidate cultural heritage stones and buildings, should be explored. 6. Moonmilk Formation Moonmilk formation has been discussed in the literature for a long time [150,163–168]. The question: Is moonmilk an abiotic process driven physicochemically, or is it biotic, mediated by microorganisms? A biological origin currently prevails; even a combination of physicochemical and biogenic processes is being considered [166]. Cañaveras et al. [150,165] indicated that bacteria inﬂuenced the physicochemistry of calcite precipitation. They ob- served that cave moonmilk comprises a network of calcite crystals and active ﬁlamentous bacteria. They also found that hydromagnesite and needle-ﬁbre aragonite deposits were associated with bacteria in Altamira Cave, predominantly Streptomyces, for which they demonstrated their ability to precipitate calcite/vaterite in the laboratory. The association between bacteria and mineral crystals was reported in other papers and described using SEM [152,153,165,168–170]. In addition, different bacterial genera such as Agromyces, Amy- colatopsis, Brachybacterium, Nocardioides, Nocardiopsis, Paenibacillus, and Rothia precipitated vaterite/calcite and Mg-calcite [171]. Maciejewska et al. [153] found that all the Streptomyces strains tested could promote calciﬁcation and biomineralization. The metabolic activities involved in the precipita- tion were amino acids ammoniﬁcation and ureolysis, which increased environmental pH. Sanchez-Moral et al. [169] stated that microbial activity induces carbonate precipitation in the early stages of deposition. However, as carbonate accumulates, a progressive decline in microbial activity occurs, as deduced from the RNA/DNA ratio, which is used as a marker of metabolic activity. The decreased metabolic activity is due to the progressive accumulation of carbonate and bacterial entrapment in mineral deposits. The high relative abundance of Crossiella in moonmilk from different caves indicates that this genus is active in moonmilk formation (Table 1). Enzymatic processes induce this mineralization, and several enzymes have been linked to Crossiella activity in moon- milk. Martin-Pozas et al. [26] suggested that moonmilk formation is related to syntrophic Appl. Biosci. 2023, 2 202 relationships between Crossiella and nitrifying bacteria, and Cuezva et al. [27] associated Crossiella with the ability to capture CO from the atmosphere and precipitate calcium carbonate as a by-product of carbonic anhydrase action, as observed in cave moonmilk. 7. Is Moonmilk a Source of Bioactive Compounds? Caves and moonmilk are colonized by complex bacterial communities. Maciejewska et al. [153] reported that Proteobacteria was the dominant phylum of moonmilk from a Belgian cave, followed by Actinobacteria, Acidobacteria, Chloroﬂexi, Nitrospirae, Gem- matimonadetes, and Planctomycetes. These seven phyla accounted for 85.8–90.2% of the total community. Martin-Pozas et al. [26] investigated the moonmilk composition from Pindal Cave in Spain. They found that Proteobacteria and Actinobacteria dominated the community with over 30% of relative abundance for each phyla, followed by Acidobacteria, Chloroﬂexi, Planctomycetes, Gemmatimonadetes, and Nitrospirae. These phyla accounted for 93.1–93.9% of the total community. The similarities between the phyla compositions of moonmilk from two different caves are remarkable. Moonmilk from a geographically distant cave [172] and another subterranean environment [173] also showed relatively similar phyla compositions. Moonmilk has been a promising reservoir for novel bacteria producing bioactive compounds, and a few novel species have been isolated, namely Streptomyces lunaelac- tis [174], Pseudomonas karstica, and Pseudomonas spelaei [175]. Several studies have stressed the great diversity of unknown bacteria inhabiting moonmilk and the isolates’ production of bioactive compounds [176–178]. The high abundance of Actinomycetota (=Actinobacteria) and Pseudomonadota (=Pro- teobacteria) in moonmilk has prompted researchers to test a series of strategies to isolate hard-to-culture “rare actinobacteria” and discover novel bioactive compounds [13,14]. Adam et al. [176] obtained 40 isolates represented by Agromyces, Amycolatopsis, Kocuria, Micrococcus, Micromonospora, Nocardia, Streptomyces, and Rhodococcus species. The Strep- tomyces isolates displayed strong inhibitory activities against Gram-positive and Gram- negative bacteria and fungi [179]. Genome mining of Streptomyces lunaelactis revealed 42 biosynthetic gene clusters [180] and the production of the antibiotics bagremycins and lunaemycins [180,181]. The genome of Crossiella, abundant in moonmilk [26], showed the presence of a combination of gene clusters involved in synthesising different bioactive com- pounds [9]. The data suggest the possibility of ﬁnding other moonmilk bacteria involved in synthesising bioactive compounds. 8. Conclusions The genus Crossiella is widely distributed in all environments, reaching a relative abundance of up to 78% in a Sicilian cave. Its occurrence in soils, plant rhizospheres and caves is especially important. The last case is probably due to its transport to the subsurface by percolating waters. Despite this abundance, the strains isolated were scarce. The data suggest that more environmental Crossiella species are waiting to be described, apart from Crossiella cryophila and Crossiella equi. The increasing number of metagenomic sequence data from all environments offers clear opportunities to guide the isolation and cultivation of Crossiella. Therefore, further efforts are required to design suitable isolation culture media. They should consider the environmental conditions of the niches where Crossiella thrives, namely alkaline pH and high mineral concentrations. Crossiella has an important role in carbon sequestration in subterranean environments. Metagenomic studies and isolating more Crossiella strains and/or species are the only way to advance knowledge of Crossiella functions in different ecosystems. Furthermore, its role in biomineralization and moonmilk formation is also apparent. Finally, Crossiella appears to be a promising source of active compounds, and the isolated strains deserve more attention regarding their potential use in biotechnological processes. Appl. Biosci. 2023, 2 203 Supplementary Materials: The following supporting information can be downloaded at: https:// www.mdpi.com/article/10.3390/applbiosci2020014/s1, Table S1: Occurrence of the genus Crossiella in different environments. Author Contributions: Conceptualization, C.S.-J. and S.S.-M.; investigation, T.M.-P., J.L.G.-P., V.J., L.L., J.C.C., A.F.-C. and S.C.; writing—original draft preparation, C.S.-J., S.S.-M. and T.M.-P.; writing— review and editing, C.S.-J. and S.S.-M. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the projects PID2020-114978GB-I00 and PID2019-110603RB-I00. The Malaga City Council ﬁnanced data from the archaeological basement of the Thyssen Museum of Malaga through a conservation contract for this Roman site. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: All data reported in this review can be found in the relevant papers cited. Scanning electron micrographs, EDX spectra, and unpublished data are available on request from Sergio Sanchez-Moral. Acknowledgments: This is a contribution from CSIC Interdisciplinary Thematic Platform Open Heritage: Research and Society (PTI-PAIS). Conﬂicts of Interest: The authors declare no conﬂict of interest. References 1. Takahashi, A.; Hotta, K.; Saito, N.; Morioka, M.; Okami, Y.; Umezawa, H. Production of novel antibiotic, dopsisamine, by a new subspecies of Nocardiopsis mutabilis with multiple antibiotic resistance. J. Antibiot. 1986, 39, 175–183. [CrossRef] [PubMed] 2. Labeda, D.P.; Lechevalier, M.P. 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Martinet, L.; Naômé, A.; Baiwir, D.; De Pauw, E.; Mazzucchelli, G.; Rigali, S. On the risks of phylogeny-based strain prioritization for drug discovery: Streptomyces lunaelactis as a case study. Biomolecules 2020, 10, 1027. [CrossRef] [PubMed] Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

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Applied Biosciences – Multidisciplinary Digital Publishing Institute

Published: May 6, 2023

Keywords: Crossiella; biofilms; caves; moonmilk; biomineralization; rhizosphere; soils; bioactive compounds

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Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment

Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment

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Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment

Crossiella, a Rare Actinomycetota Genus, Abundant in the Environment

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