Microbial colonization of metal sulfide minerals at a diffuse-flow deep-sea hydrothermal vent at 9°50′N on the East Pacific Rise
Chloe H. Wang
Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Department of Chemistry, Haverford College, Haverford, PA, USA
Search for more papers by this authorLara K. Gulmann
Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Search for more papers by this authorTong Zhang
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
College of Environmental Science and Engineering, Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, Tianjin Key Laboratory of Environmental Remediation and Pollution Control, Nankai University, Tianjin, China
Search for more papers by this authorGabriela A. Farfan
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Department of Mineral Sciences, Smithsonian Institution, Washington, DC, USA
Search for more papers by this authorCorresponding Author
Colleen M. Hansel
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Correspondence
Colleen M. Hansel, Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: chansel@whoi.edu
Stefan M. Sievert, Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: ssievert@whoi.edu
Search for more papers by this authorCorresponding Author
Stefan M. Sievert
Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Correspondence
Colleen M. Hansel, Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: chansel@whoi.edu
Stefan M. Sievert, Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: ssievert@whoi.edu
Search for more papers by this authorChloe H. Wang
Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Department of Chemistry, Haverford College, Haverford, PA, USA
Search for more papers by this authorLara K. Gulmann
Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Search for more papers by this authorTong Zhang
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
College of Environmental Science and Engineering, Ministry of Education Key Laboratory of Pollution Processes and Environmental Criteria, Tianjin Key Laboratory of Environmental Remediation and Pollution Control, Nankai University, Tianjin, China
Search for more papers by this authorGabriela A. Farfan
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Department of Mineral Sciences, Smithsonian Institution, Washington, DC, USA
Search for more papers by this authorCorresponding Author
Colleen M. Hansel
Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Correspondence
Colleen M. Hansel, Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: chansel@whoi.edu
Stefan M. Sievert, Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: ssievert@whoi.edu
Search for more papers by this authorCorresponding Author
Stefan M. Sievert
Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA, USA
Correspondence
Colleen M. Hansel, Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: chansel@whoi.edu
Stefan M. Sievert, Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543, USA.
Email: ssievert@whoi.edu
Search for more papers by this authorAbstract
Metal sulfide minerals, including mercury sulfides (HgS), are widespread in hydrothermal vent systems where sulfur-oxidizing microbes are prevalent. Questions remain as to the impact of mineral composition and structure on sulfur-oxidizing microbial populations at deep-sea hydrothermal vents, including the possible role of microbial activity in remobilizing elemental Hg from HgS. In the present study, metal sulfides varying in metal composition, structure, and surface area were incubated for 13 days on and near a diffuse-flow hydrothermal vent at 9°50′N on the East Pacific Rise. Upon retrieval, incubated minerals were examined by scanning electron microscopy with energy-dispersive X-ray spectroscopy (SEM-EDS), X-ray diffraction (XRD), and epifluorescence microscopy (EFM). DNA was extracted from mineral samples, and the 16S ribosomal RNA gene sequenced to characterize colonizing microbes. Sulfur-oxidizing genera common to newly exposed surfaces (Sulfurimonas, Sulfurovum, and Arcobacter) were present on all samples. Differences in their relative abundance between and within incubation sites point to constraining effects of the immediate environment and the minerals themselves. Greater variability in colonizing community composition on off-vent samples suggests that the bioavailability of mineral-derived sulfide (as influenced by surface area, crystal structure, and reactivity) exerted greater control on microbial colonization in the ambient environment than in the vent environment, where dissolved sulfide is more abundant. The availability of mineral-derived sulfide as an electron donor may thus be a key control on the activity and proliferation of deep-sea chemosynthetic communities, and this interpretation supports the potential for microbial dissolution of HgS at hydrothermal vents.
Supporting Information
Filename | Description |
---|---|
gbi12396-sup-0001-Supinfo.pdfPDF document, 18 MB | Supinfo |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Auvray, P., & Genet, F. (1973). Affinement de la structure crystalline du cinabre α-HgS. Bulletin De La Societe Francaise De Mineralogie Et De Cristallographie, 96, 218–219.
- Baldi, F., & Olson, G. J. (1987). Effects of cinnabar on pyrite oxidation by Thiobacillus ferrooxidans and cinnabar mobilization by a mercury-resistant strain. Applied and Environmental Microbiology, 53(4), 772–776. https://doi.org/10.1128/AEM.53.4.772-776.1987
- Brostigen, G., Kjekshus, A., & Chr, R. (1973). Compounds with the marcasite type crystal structure. Acta Chemica Scandinavica, 27, 2791–2796.
- Cameron, T. S., Decken, A., Dionne, I., Fang, M., Krossing, I., & Passmore, J. (2002). Approaching the gas-phase structures of [AgS8]+ and [AgS16]+ in the solid state. Chemistry – A European Journal, 8(15), 3386–3401. https://doi.org/10.1002/1521-3765(20020802)8:15<3386:AID-CHEM3386>3.0.CO;2-9
10.1002/1521-3765(20020802)8:15<3386::AID-CHEM3386>3.0.CO;2-9 CASPubMedWeb of Science®Google Scholar
- Campbell, B. J., Polson, S. W., Zeigler Allen, L., Williamson, S. J., Lee, C. K., Wommack, K. E., & Cary, S. C. (2013). Diffuse flow environments within basalt- and sediment-based hydrothermal vent ecosystems harbor specialized microbial communities. Frontiers in Microbiology, 4, 182. https://doi.org/10.3389/fmicb.2013.00182
- Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., … Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7(5), 335–336. https://doi.org/10.1038/nmeth.f.303
- Crespo-Medina, M., Chatziefthimiou, A. D., Bloom, N. S., Luther, G. W. I. I. I., Wright, D. D., Reinfelder, J. R., … Barkay, T. (2009). Adaptation of chemosynthetic microorganisms to elevated mercury concentrations in deep-sea hydrothermal vents. Limnology and Oceanography, 54(1), 41–49. https://doi.org/10.4319/lo.2009.54.1.0041
- Dyrssen, D. (1989). Biogenic sulfur in two different marine environments. Marine Chemistry, 28(1), 241–249. https://doi.org/10.1016/0304-4203(89)90198-9
- Edgar, R. C. (2010). Search and clustering orders of magnitude faster than BLAST. Bioinformatics (Oxford, England), 26(19), 2460–2461. https://doi.org/10.1093/bioinformatics/btq461
- Edwards, K. J., Bond, P. L., & Banfield, J. F. (2000). Characteristics of attachment and growth of Thiobacillus caldus on sulphide minerals: A chemotactic response to sulphur minerals? Environmental Microbiology, 2(3), 324–332. https://doi.org/10.1046/j.1462-2920.2000.00111.x
- Finklea, S. L., Cathey, L., & Amma, E. L. (1976). Investigation of the bonding mechanism in pyrite using the Mössbauer effect and X-ray crystallography. Acta Crystallographica Section A: Crystal Physics, Diffraction, Theoretical and General Crystallography, 32(4), 529–537. https://doi.org/10.1107/S0567739476001198
10.1107/S0567739476001198 Google Scholar
- Finster, K., Liesack, W., & Tindall, B. J. (1997). Sulfurospirillum arcachonense sp. Nov., a new microaerophilic sulfur-reducing bacterium. International Journal of Systematic Bacteriology, 47(4), 1212–1217. https://doi.org/10.1099/00207713-47-4-1212
- Fortunato, C. S., & Huber, J. A. (2016). Coupled RNA-SIP and metatranscriptomics of active chemolithoautotrophic communities at a deep-sea hydrothermal vent. ISME Journal, 10(8), 1925–1938. https://doi.org/10.1038/ismej.2015.258
- Fortunato, C. S., Larson, B., Butterfield, D. A., & Huber, J. A. (2018). Spatially distinct, temporally stable microbial populations mediate biogeochemical cycling at and below the seafloor in hydrothermal vent fluids: Microbial genomics at axial seamount. Environmental Microbiology, 20(2), 769–784. https://doi.org/10.1111/1462-2920.14011
- Gulmann, L. K., Beaulieu, S. E., Shank, T. M., Ding, K., Seyfried, W. E., & Sievert, S. M. (2015). Bacterial diversity and successional patterns during biofilm formation on freshly exposed basalt surfaces at diffuse-flow deep-sea vents. Frontiers in Microbiology, 6, 901. https://doi.org/10.3389/fmicb.2015.00901
- Haas, B. J., Gevers, D., Earl, A. M., Feldgarden, M., Ward, D. V., Giannoukos, G., … Birren, B. W. (2011). Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Research, 21(3), 494–504. https://doi.org/10.1101/gr.112730.110
- Hanawalt, J. D., Rinn, H. W., & Frevel, L. K. (1938). Chemical analysis by X-Ray diffraction. Industrial & Engineering Chemistry Analytical Edition, 10(9), 457–512. https://doi.org/10.1021/ac50125a001
- Holden, J. F., Breier, J. A., Rogers, K. L., Schulte, M. D., & Toner, B. M. (2012). Biogeochemical processes at hydrothermal vents: Microbes and minerals, bioenergetics, and carbon fluxes. Oceanography, 25(1), 196–208. https://doi.org/10.2307/24861158
- Holley, E. A., McQuillan, J.A., Craw, D., Kim, J. P., & Sander, S. G. (2007). Mercury mobilization by oxidative dissolution of cinnabar (α-HgS) and metacinnabar (β-HgS). Chemical Geology, 240(3–4), 313–325. https://doi.org/10.1016/j.chemgeo.2007.03.001
- Inagaki, F., Takai, K., Kabayashi, H., Nealson, K.H., & Horikoshi, K. (2003). Sulfurimonas autotrophica gen. nov., sp. nov., a novel sulfur-oxidizing Epsilon-proteobacterium isolated from hydrothermal sediments in the Mid-Okinawa Trough. International Journal of Systematic and Evolutionary Microbiology, 53(6), 1801–1805. https://doi.org/10.1099/ijs.0.02682-0
- Inagaki, F., Takai, K., Nealson, K.H., & Horikoshi, K. (2004). Sulfurovum lithotrophicum gen. nov., sp. nov., a novel sulfur-oxidizing chemolithoautotroph within the Epsilon-Proteobacteria isolated from Okinawa Trough hydrothermal sediments. International Journal of Systematic and Evolutionary Microbiology, 54(5), 1477–1482. https://doi.org/10.1099/ijs.0.03042-0
- Jannasch, H. W., & Mottl, M. J. (1985). Geomicrobiology of deep-sea hydrothermal vents. Science, 229(4715), 717–725. https://doi.org/10.1126/science.229.4715.717
- Kube, M., Chernikova, T. N., Al-Ramahi, Y., Beloqui, A., Lopez-Cortez, N., Guazzaroni, M.-E., … Golyshin, P. N. (2013). Genome sequence and functional genomic analysis of the oil-degrading bacterium Oleispira antarctica. Nature Communications, 4, 2156. https://doi.org/10.1038/ncomms3156
- Le Bris, N., Govenar, B., Le Gall, C., & Fisher, C. R. (2006). Variability of physico-chemical conditions in 9°50′N EPR diffuse flow vent habitats. Marine Chemistry, 98(2–4), 167–182. https://doi.org/10.1016/j.marchem.2005.08.008
- Lehmann, W. M. (1924). XIX. Röntgenographische Untersuchungen an natürlichem und synthetischem Metacinnabarit (HgS). Zeitschrift Für Kristallographie – Crystalline Materials, 60(1–6), 379–413. https://doi.org/10.1524/zkri.1924.60.1.379
- Lozupone, C., Lladser, M. E., Knights, D., Stombaugh, J., & Knight, R. (2011). UniFrac: An effective distance metric for microbial community comparison. ISME Journal, 5, 169–172. https://doi.org/10.1038/ismej.2010.133
- Mason, O. U., Han, J., Woyke, T., & Jansson, J. K. (2014). Single-cell genomics reveals features of a Colwellia species that was dominant during the Deepwater Horizon oil spill. Frontiers in Microbiology, 5, 332. https://doi.org/10.3389/fmicb.2014.00332
- Mason, R. P., Choi, A. L., Fitzgerald, W. F., Hammerschmidt, C. R., Lamborg, C. H., Soerensen, A. L., & Sunderland, E. M. (2012). Mercury biogeochemical cycling in the ocean and policy implications. Environmental Research, 119, 101–117. https://doi.org/10.1016/j.envres.2012.03.013
- McGuire, M. M., Edwards, K. J., Banfield, J. F., & Hamers, R. J. (2001). Kinetics, surface chemistry, and structural evolution of microbially mediated sulfide mineral dissolution. Geochimica Et Cosmochimica Acta, 65(8), 1243–1258. https://doi.org/10.1016/S0016-7037(00)00601-3
- McNichol, J., Stryhanyuk, H., Sylva, S. P., Thomas, F., Musat, N., Seewald, J. S., & Sievert, S. M. (2018). Primary productivity below the seafloor at deep-sea hot springs. Proceedings of the National Academy of Sciences, 115(26), 6756–6761. https://doi.org/10.1073/pnas.1804351115
- Meier, D. V., Pjevac, P., Bach, W., Hourdez, S., Girguis, P. R., Vidoudez, C., … Meyerdierks, A. (2017). Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents. ISME Journal, 11(7), 1545–1558. https://doi.org/10.1038/ismej.2017.37
- Mino, S., Kudo, H., Arai, T., Sawabe, T., Takai, K., & Nakagawa, S. (2014). Sulfurovum aggregans sp. Nov., a hydrogen-oxidizing, thiosulfate-reducing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent chimney, and an emended description of the genus Sulfurovum. International Journal of Systematic and Evolutionary Microbiology, 64(Pt 9), 3195–3201. https://doi.org/10.1099/ijs.0.065094-0
- Moussard, H., Corre, E., Cambon-Bonavita, M.-A., Fouquet, Y., & Jeanthon, C. (2006). Novel uncultured Epsilonproteobacteria dominate a filamentous sulphur mat from the 13°N hydrothermal vent field, East Pacific Rise. FEMS Microbiology Ecology, 58(3), 449–463. https://doi.org/10.1111/j.1574-6941.2006.00192.x
- Nakagawa, S., Inagaki, F., Takai, K., Horikoshi, K., & Sako, Y. (2005). Thioreductor micantisoli gen. nov., sp. nov., a novel mesophilic, sulfur-reducing chemolithoautotroph within the Epsilon-Proteobacteria isolated from hydrothermal sediments in the Mid-Okinawa Trough. International Journal of Systematic and Evolutionary Microbiology, 55(2), 599–605. https://doi.org/10.1099/ijs.0.63351-0
- O'Brien, C. E., Giovannelli, D., Govenar, B., Luther, G. W., Lutz, R. A., Shank, T. M., & Vetriani, C. (2015). Microbial biofilms associated with fluid chemistry and megafaunal colonization at post-eruptive deep-sea hydrothermal vents. Deep Sea Research Part II: Topical Studies in Oceanography, 121, 31–40. https://doi.org/10.1016/j.dsr2.2015.07.020
- Orcutt, B. N., Sylvan, J. B., Knab, N. J., & Edwards, K. J. (2011). Microbial ecology of the Dark Ocean above, at, and below the seafloor. Microbiology and Molecular Biology Reviews, 75(2), 361–422. https://doi.org/10.1128/MMBR.00039-10
- Pfennig, N., & Biebl, H. (1976). Desulfuromonas acetoxidans gen. Nov. And sp. Nov., a new anaerobic, sulfur-reducing, acetate-oxidizing bacterium. Archives of Microbiology, 110(1), 3–12. https://doi.org/10.1007/BF00416962
- Pjevac, P., Kamyshny, A., Dyksma, S., & Mußmann, M. (2014). Microbial consumption of zero-valence sulfur in marine benthic habitats. Environmental Microbiology, 16(11), 3416–3430. https://doi.org/10.1111/1462-2920.12410
- Pjevac, P., Meier, D. V., Markert, S., Hentschker, C., Schweder, T., Becher, D., … Meyerdierks, A. (2018). Metaproteogenomic profiling of microbial communities colonizing actively venting hydrothermal chimneys. Frontiers in Microbiology, 9, 680. https://doi.org/10.3389/fmicb.2018.00680
- Pósfai, M., & Dunin-Borkowski, R. E. (2006). Sulfides in biosystems. Reviews in Mineralogy and Geochemistry, 61(1), 679–714. https://doi.org/10.2138/rmg.2006.61.13
- Sievert, S., & Vetriani, C. (2012). Chemoautotrophy at deep-sea vents: Past, present, and future. Oceanography, 25(1), 218–233. https://doi.org/10.5670/oceanog.2012.21
- Sievert, S. M., Wieringa, E. B. A., Wirsen, C. O., & Taylor, C. D. (2007). Growth and mechanism of filamentous-sulfur formation by Candidatus Arcobacter sulfidicus in opposing oxygen-sulfide gradients. Environmental Microbiology, 9(1), 271–276. https://doi.org/10.1111/j.1462-2920.2006.01156.x
- Stokke, R., Dahle, H., Roalkvam, I., Wissuwa, J., Daae, F. L., Tooming-Klunderud, A., … Steen, I. H. (2015). Functional interactions among filamentous Epsilonproteobacteria and Bacteroidetes in a deep-sea hydrothermal vent biofilm: Deep-sea vent filamentous Epsilonproteobacteria. Environmental Microbiology, 17(10), 4063–4077. https://doi.org/10.1111/1462-2920.12970
- Strathmann, M., Wingender, J., & Flemming, H.-C. (2002). Application of fluorescently labelled lectins for the visualization and biochemical characterization of polysaccharides in biofilms of Pseudomonas aeruginosa. Journal of Microbiological Methods, 50, 237–248. https://doi.org/10.1016/S0167-7012(02)00032-5
- Takai, K., Suzuki, M., Nakagawa, S., Miyazaki, M., Suzuki, Y., Inagaki, F., & Hiroshi, F. (2006). Sulfurimonas paralvinellae sp. nov., a novel mesophilic, hydrogen- and sulfur-oxidizing chemolithoautotroph within the Epsilonproteobacteria isolated from a deep-sea hydrothermal vent polychaete nest, reclassification of Thiomicrospira denitrificans as Sulfurimonas denitrificans comb. nov. and emended description of the genus Sulfurimonas. International Journal of Systematic and Evolutionary Microbiology, 56(8), 1725–1733. https://doi.org/10.1099/ijs.0.64255-0
- Taylor, C. D., & Wirsen, C. O. (1997). Microbiology and ecology of filamentous sulfur formation. Science, 277, 1483–1485. https://doi.org/10.1126/science.277.5331.1483
- Taylor, C. D., Wirsen, C. O., & Gaill, F. (1999). Rapid microbial production of filamentous sulfur mats at hydrothermal vents. Applied and Environmental Microbiology, 65(5), 2253–2255. https://doi.org/10.1128/AEM.65.5.2253-2255.1999
- Templeton, A. S., Knowles, E. J., Eldridge, D. L., Arey, B. W., Dohnalkova, A. C., Webb, S. M., … Staudigel, H. (2009). A seafloor microbial biome hosted within incipient ferromanganese crusts. Nature Geoscience, 2(12), 872–876. https://doi.org/10.1038/ngeo696
- Toner, B. M., Lesniewski, R. A., Marlow, J. J., Briscoe, L. J., Santelli, C. M., Bach, W., … Edwards, K. J. (2013). Mineralogy drives bacterial biogeography of hydrothermally inactive seafloor sulfide deposits. Geomicrobiology Journal, 30(4), 313–326. https://doi.org/10.1080/01490451.2012.688925
- Varekamp, J. C., & Buseck, P. R. (1984). The speciation of mercury in hydrothermal systems, with applications to ore deposition. Geochimica Et Cosmochimica Acta, 48(1), 177–185. https://doi.org/10.1016/0016-7037(84)90359-4
- Vázquez-Rodríguez, A. I. (2014). Microbial colonization and dissolution of mercury sulfide minerals. PhD Thesis. Cambridge, MA: Harvard University.
- Vázquez-Rodríguez, A. I., Hansel, C. M., Zhang, T., Lamborg, C. H., Santelli, C. M., Webb, S. M., & Brooks, S. C. (2015). Microbial- and thiosulfate-mediated dissolution of mercury sulfide minerals and transformation to gaseous mercury. Frontiers in Microbiology, 6, 596. https://doi.org/10.3389/fmicb.2015.00596
- Vetriani, C., Chew, Y. S., Miller, S. M., Yagi, J., Coombs, J., Lutz, R. A., & Barkay, T. (2005). Mercury adaptation among bacteria from a deep-sea hydrothermal vent. Applied and Environmental Microbiology, 71(1), 220–226. https://doi.org/10.1128/AEM.71.1.220-226.2005
- Waite, D. W., Vanwonterghem, I., Rinke, C., Parks, D. H., Zhang, Y., Takai, K., … Hugenholtz, P. (2018). Addendum: comparative genomic analysis of the Class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. nov.). Frontiers in Microbiology, 9, 772. https://doi.org/10.3389/fmicb.2018.00772
- Waite, D. W., Vanwonterghem, I., Rinke, C., Parks, D. H., Zhang, Y., Takai, K., & Hugenholtz, P. (2017). Comparative genomic analysis of the class Epsilonproteobacteria and proposed reclassification to Epsilonbacteraeota (phyl. Nov.). Frontiers in Microbiology, 8, 682. https://doi.org/10.3389/fmicb.2017.00682
- Wirsen, C. O., Sievert, S. M., Cavanaugh, C. M., Molyneaux, S. J., Ahmad, A., Taylor, L. T., … Taylor, C. D. (2002). Characterization of an autotrophic sulfide-oxidizing marine Arcobacter sp. that produces filamentous sulfur. Applied Environmental Microbiology, 68(1), 316–325. https://doi.org/10.1128/AEM.68.1.316-325.2002
- Yamamoto, M., Nakagawa, S., Shimamura, S., Takai, K., & Horikoshi, K. (2010). Molecular characterization of inorganic sulfur-compound metabolism in the deep-sea epsilonproteobacterium Sulfurovum sp. NBC37-1. Environmental Microbiology, 12(5), 1144–1153. https://doi.org/10.1111/j.1462-2920.2010.02155.x