Research progress in microbial-mediated sulfur cycles in geothermal habitats: Insights into biological processes on the early Earth

doi:10.13745/j.esf.sf.2022.2.82

Abstract

Abstract:

Geothermal habitats are characterized by high temperature and hypoxia similar to the conditions of early Earth. Therefore, thermophiles in modern geothermal habitats can be used to study the co-evolution of life and environment on the early Earth. The sulfur cycle is one of main biogeochemical processes on the early Earth, thus studying microbial-mediated sulfur cycle and its coupling with other elements in geothermal habitats can deepen our understanding of the biogeochemical sulfur cycle and its environmental effects on the early Earth. This review summarizes the characteristics of microbial diversity in the sulfur cycle and their influencing factors in geothermal habitats, as well as the coupling of the sulfur cycle with the iron, methane, and nitrogen cycles. Combined with Archean geochemical conditions and stratigraphic isotope record, this review also discusses the possible environmental effects of the sulfur cycle on the early Earth. Finally, an outlook on future research on microbial-mediated co-evolution of the sulfur cycle and environment on the early Earth is discussed.

Key words: geothermal habitats, sulfur cycle, Archean, microbes, environmental effect

CLC Number:

P597

MA Li, XIE Yihao, WU Geng, JIANG Hongchen. Research progress in microbial-mediated sulfur cycles in geothermal habitats: Insights into biological processes on the early Earth[J]. Earth Science Frontiers, 2023, 30(2): 479-494.

Figures/Tables 4

References 146

[15]	BOYD E S, FECTEAU K M, HAVIG J R, et al. Modeling the habitat range of phototrophs in Yellowstone National Park: toward the development of a comprehensive fitness landscape[J]. Frontiers in Microbiology, 2012, 3: 221. DOI PMID
[16]	COX A, SHOCK E L, HAVIG J R. The transition to microbial photosynthesis in hot spring ecosystems[J]. Chemical Geology, 2011, 280(3/4): 344-351. DOI URL
[17]	GEORGIEVA M N, LITTLE C T S, MASLENNIKOV V V, et al. The history of life at hydrothermal vents[J]. Earth-Science Reviews, 2021, 217: 103602. DOI URL
[18]	HAVIG J R, HAMILTON T L, BACHAN A, et al. Sulfur and carbon isotopic evidence for metabolic pathway evolution and a four-stepped Earth system progression across the Archean and Paleoproterozoic[J]. Earth-Science Reviews, 2017, 174: 1-21. DOI URL
[19]	WU B, LIU F F, FANG W W, et al. Microbial sulfur metabolism and environmental implications[J]. Science of the Total Environment, 2021, 778: 146085. DOI URL
[20]	FAKHRAEE M, KATSEV S. Organic sulfur was integral to the Archean sulfur cycle[J]. Nature Communications, 2019, 10: 4556. DOI PMID
[21]	MUYZER G, STAMS A J M. The ecology and biotechnology of sulphate-reducing bacteria[J]. Nature Reviews Microbiology, 2008, 6(6): 441-454. DOI PMID
[22]	GILLEAUDEAU G J, KAH L C. Heterogeneous redox conditions and a shallow chemocline in the Mesoproterozoic Ocean: evidence from carbon-sulfur-iron relationships[J]. Precambrian Research, 2015, 257: 94-108. DOI URL
[23]	CANFIELD D E, RAISWELL R. The evolution of the sulfur cycle[J]. American Journal of Science, 1999, 299(7/8/9): 697-723. DOI URL
[24]	COCKELL C S, RAVEN J A. Ozone and life on the Archaean earth[J]. Philosophical Transactions Mathematical Physical and Engineering Sciences, 2007, 365(1856): 1889-1901.
[25]	DODD M S, PAPINEAU D, GRENNE T, et al. Evidence for early life in Earth’s oldest hydrothermal vent precipitates[J]. Nature, 2017, 543(7643): 60-64. DOI URL
[26]	NISBET E G, SLEEP N H. The habitat and nature of early life[J]. Nature, 2001, 409(6823): 1083-1091. DOI URL
[27]	ROBERT F, CHAUSSIDON M. A palaeotemperature curve for the Precambrian oceans based on silicon isotopes in cherts[J]. Nature, 2006, 443(7114): 969-972. DOI URL
[28]	KNAUTH L P. Temperature and salinity history of the Precambrian Ocean: implications for the course of microbial evolution[J]. Palaeogeography, Palaeoclimatology, Palaeoecology, 2005, 219(1/2): 53-69. DOI URL
[29]	GAUCHER E A, GOVINDARAJAN S, GANESH O K. Palaeotemperature trend for Precambrian life inferred from resurrected proteins[J]. Nature, 2008, 451(7179): 704-707. DOI URL
[30]	FRALICK P, CARTER J E. Neoarchean deep marine paleotemperature: evidence from turbidite successions[J]. Precambrian Research, 2011, 191(1/2): 78-84. DOI URL
[31]	VAN DEN BOORN S H J M, VAN BERGEN M J, NIJMAN W, et al. Dual role of seawater and hydrothermal fluids in Early Archean chert formation: evidence from silicon isotopes[J]. Geology, 2007, 35(10): 939-942. DOI URL
[32]	BLAKE R E, CHANG S J, LEPLAND A. Phosphate oxygen isotopic evidence for a temperate and biologically active Archaean Ocean[J]. Nature, 2010, 464(7291): 1029-1032. DOI URL
[1]	CICCARELLI F D, DOERKS T, VON MERING C, et al. Toward automatic reconstruction of a highly resolved tree of life[J]. Science, 2006, 311(5765): 1283-1287. DOI PMID
[2]	BROWN J R, DOUADY C J, ITALIA M J, et al. Universal trees based on large combined protein sequence data sets[J]. Nature Genetics, 2001, 28(3): 281-285. DOI PMID
[3]	HUA Z S, WANG Y L, EVANS P N, et al. Insights into the ecological roles and evolution of methyl-coenzyme M reductase-containing hot spring Archaea[J]. Nature Communications, 2019, 10: 4574. DOI URL
[4]	YANG Y Y, ZHANG C L, LENTON T M, et al. The evolution pathway of ammonia-oxidizing Archaea shaped by major geological events[J]. Molecular Biology and Evolution, 2021, 38(9): 3637-3648. DOI PMID
[5]	DI GIULIO M. The universal ancestor lived in a thermophilic or hyperthermophilic environment[J]. Journal of Theoretical Biology, 2000, 203(3): 203-213. PMID
[6]	MARTIN W, BAROSS J, KELLEY D, et al. Hydrothermal vents and the origin of life[J]. Nature Reviews Microbiology, 2008, 6(11): 805-814. DOI PMID
[7]	AMENABAR M J, BOYD E S. A review of the mechanisms of mineral-based metabolism in early Earth analog rock-hosted hydrothermal ecosystems[J]. World Journal of Microbiology and Biotechnology, 2019, 35(2): 29. DOI PMID
[8]	KASTING J F. Earth’s early atmosphere[J]. Science, 1993, 259(5097): 920-926. DOI URL
[9]	KASTING J F, SIEFERT J L. Life and the evolution of Earth’s atmosphere[J]. Science, 2002, 296(5570): 1066-1068. DOI URL
[10]	WANG S, HOU W G, DONG H L, et al. Control of temperature on microbial community structure in hot springs of the Tibetan Plateau[J]. PLoS One, 2013, 8(5): e62901. DOI URL
[11]	WU G, JIANG H C, DONG H L, et al. Distribution of arsenite- oxidizing bacteria and its correlation with temperature in hot springs of the Tibetan- Yunnan geothermal zone in Western China[J]. Geomicrobiology Journal, 2015, 32(6): 482-493. DOI URL
[12]	BOYD E S, HAMILTON T L, SPEAR J R, et al. FeFe -hydrogenase in Yellowstone National Park: evidence for dispersal limitation and phylogenetic niche conservatism[J]. The ISME Journal, 2010, 4(12): 1485-1495. DOI URL
[13]	ADAM N, PERNER M. Microbially mediated hydrogen cycling in deep-sea hydrothermal vents[J]. Frontiers in Microbiology, 2018, 9: 2873. DOI PMID
[14]	JØRGENSEN B B, BOETIUS A. Feast and famine—microbial life in the deep-sea bed[J]. Nature Reviews Microbiology, 2007, 5(10): 770-781. DOI URL
[33]	GARCIA A K, SCHOPF J W, YOKOBORI S I, et al. Reconstructed ancestral enzymes suggest long-term cooling of Earth’s photic zone since the Archean[J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(18): 4619-4624.
[34]	KELLER M A, KAMPJUT D, HARRISON S A, et al. Sulfate radicals enable a non-enzymatic Krebs cycle precursor[J]. Nature Ecology and Evolution, 2017, 1(4): 83. DOI PMID
[35]	KRISSANSEN-TOTTON J, ARNEY G N, CATLING D C. Constraining the climate and ocean pH of the early Earth with a geological carbon cycle model[J]. Proceedings of the National Academy of Sciences of the United States of America, 2018, 115(16): 4105-4110.
[36]	李超, 程猛, ALGEO T J, 等. 早期地球海洋水化学分带的理论预测[J]. 中国科学: 地球科学, 2015, 45(12): 1829-1838.
[37]	CATLING D C, ZAHNLE K J. The Archean atmosphere[J]. Science Advances, 2020, 6(9): eaax1420.
[38]	KUMP L R, SEYFRIED W E Jr. Hydrothermal Fe fluxes during the Precambrian: effect of low oceanic sulfate concentrations and low hydrostatic pressure on the composition of black smokers[J]. Earth and Planetary Science Letters, 2005, 235(3/4): 654-662. DOI URL
[39]	FAKHRAEE M, CROWE S A, KATSEV S. Sedimentary sulfur isotopes and neoarchean ocean oxygenation[J]. Science Advances, 2018, 4(1): e1701835.
[40]	FAKHRAEE M, HANCISSE O, CANFIELD D E, et al. Proterozoic seawater sulfate scarcity and the evolution of ocean-atmosphere chemistry[J]. Nature Geoscience, 2019, 12(5): 375-380. DOI URL
[41]	KONHAUSER K O, PECOITS E, LALONDE S V, et al. Oceanic nickel depletion and a methanogen famine before the Great Oxidation Event[J]. Nature, 2009, 458(7239): 750-753. DOI URL
[42]	PAULO L M, STAMS A J M, SOUSA D Z. Methanogens, sulphate and heavy metals: a complex system[J]. Reviews in Environmental Science and Bio-Technology, 2015, 14(4): 537-553.
[43]	TOPUOGLU B D, MEYDAN C, NGUYEN T B, et al. Growth kinetics, carbon isotope fractionation, and gene expression in the Hyperthermophile methanocaldococcus jannaschii during hydrogen-limited growth and inter species hydrogen transfer[J]. Applied and Environmental Microbiology, 2019, 85(9): e00180-e00190.
[44]	ZHANG Y M, WU G, JIANG H C, et al. Abundant and rare microbial biospheres respond differently to environmental and spatial factors in Tibetan hot springs[J]. Frontiers in Microbiology, 2018, 9: 2096. DOI PMID
[45]	刘阳, 姜丽晶, 邵宗泽. 硫氧化细菌的种类及硫氧化途径的研究进展[J]. 微生物学报, 2018, 58(2): 191-201.
[46]	陈俊松, 杨渐, 蒋宏忱. 湖泊硫循环微生物研究进展[J]. 微生物学报, 2020, 60(6): 1177-1191.
[47]	TIAN H M, GAO P K, CHEN Z H, et al. Compositions and abundances of sulfate-reducing and sulfur-oxidizing microorganisms in water-flooded petroleum reservoirs with different temperatures in China[J]. Frontiers in Microbiology, 2017, 8: 143. DOI PMID
[48]	CAO H L, WANG Y, LEE O O, et al. Microbial sulfur cycle in two hydrothermal chimneys on the Southwest Indian Ridge[J]. MBio, 2014, 5(1): e00980-e00913.
[49]	甄莉, 吴耿, 杨渐, 等. 西藏热泉沉积物的硫氧化细菌多样性及其影响因素[J]. 微生物学报, 2019, 59(6): 1089-1104.
[50]	张宏, 李颖杰, 王文颖, 等. 微生物硫循环网络的研究进展[J]. 微生物学报, 2021, 61(6): 1567-1581.
[51]	MEIER D V, PJEVAC P, BACH W, et al. Niche partitioning of diverse sulfur-oxidizing bacteria at hydrothermal vents[J]. The ISME Journal, 2017, 11(7): 1545-1558. DOI URL
[52]	GIOVANNELLI D, SIEVERT S M, HÜGLER M, et al. Insight into the evolution of microbial metabolism from the deep-branching bacterium, Thermovibrio ammonificans[J]. elife, 2017, 6: e18990. DOI URL
[53]	EVERROAD R C, OTAKI H, MATSUURA K, et al. Diversification of bacterial community composition along a temperature gradient at a thermal spring[J]. Microbes and Environments, 2012, 27(4): 374-381. DOI PMID
[54]	CZAJA A D, BEUKES N J, OSTERHOUT J T. Sulfur-oxidizing bacteria prior to the Great Oxidation Event from the 2.52 Ga Gamohaan Formation of South Africa[J]. Geology, 2016, 44(12): 983-986. DOI URL
[55]	JAVAUX E J, MARSHALL C P, BEKKER A. Organic-walled microfossils in 3.2-billion-year-old shallow-marine siliciclastic deposits[J]. Nature, 2010, 463(7283): 934-938. DOI URL
[56]	KAPPLER A, PASQUERO C, KONHAUSER K O, et al. Deposition of banded iron formations by anoxygenic phototrophic Fe(II)-oxidizing bacteria[J]. Geology, 2005, 33(11): 865-868. DOI URL
[57]	LEPOT K. Signatures of early microbial life from the Archean (4 to 2.5 Ga) eon[J]. Earth-Science Reviews, 2020, 209: 103296. DOI URL
[58]	BÜHRING S I, SIEVERT S M, JONKERS H M, et al. Insights into chemotaxonomic composition and carbon cycling of phototrophic communities in an artesian sulfur-rich spring (Zodletone, Oklahoma, USA), a possible analog for ancient microbial mat systems[J]. Geobiology, 2011, 9(2): 166-179. DOI PMID
[59]	HAMILTON T L, BENNETT A C, MURUGAPIRAN S K, et al. Anoxygenic phototrophs span geochemical gradients and diverse morphologies in terrestrial geothermal springs[J]. mSystems, 2019, 4(6): e00498-e00419.
[60]	KALASHNIKOV A M, GAISIN V A, SUKHACHEVA M V, et al. Anoxygenic phototrophic bacteria from microbial communities of Goryachinsk Thermal Spring (Baikal Area, Russia)[J]. Microbiology, 2014, 83(4): 407-421. DOI URL
[61]	KAWAI S, KAMIYA N, MATSUURA K, et al. Symbiotic growth of a thermophilic sulfide-oxidizing photoautotroph and an elemental sulfur-disproportionating chemolithoautotroph and cooperative dissimilatory oxidation of sulfide to sulfate[J]. Frontiers in Microbiology, 2019, 10: 1150. DOI PMID
[62]	AKIMOV V N, PODOSOKORSKAYA O A, SHLYAPNIKOV M G, et al. Dominant phylotypes in the 16S rRNA gene clone libraries from bacterial mats of the Uzon caldera (Kamchatka, Russia) hydrothermal springs[J]. Microbiology, 2013, 82(6): 721-727. DOI URL
[63]	BENNETT A C, MURUGAPIRAN S K, HAMILTON T L. Temperature impacts community structure and function of phototrophic Chloroflexi and Cyanobacteria in two alkaline hot springs in Yellowstone National Park[J]. Environmental Microbiology Reports, 2020, 12(5): 503-513. DOI URL
[64]	REINHARD C T, RAISWELL R, SCOTT C, et al. A late Archean sulfidic sea stimulated by early oxidative weathering of the continents[J]. Science, 2009, 326(5953): 713-716. DOI PMID
[65]	CANFIELD D E, JØRGENSEN B B, FOSSING H, et al. Pathways of organic carbon oxidation in three continental margin sediments[J]. Marine Geology, 1993, 113(1/2): 27-40. DOI URL
[66]	PIRES R H, LOURENÇO A I, MORAIS F, et al. A novel membrane-bound respiratory complex from Desulfovibrio desulfuricans ATCC 27774[J]. Biochimica et Biophysica Acta-Bioenergetics, 2003, 1605(1/2/3): 67-82. DOI URL
[67]	PEREIRA I A C, RAMOS A R, GREIN F, et al. A comparative genomic analysis of energy metabolism in sulfate reducing bacteria and Archaea[J]. Frontiers in Microbiology, 2011, 2: 69. DOI PMID
[68]	LELOUP J, FOSSING H, KOHLS K, et al. Sulfate-reducing bacteria in marine sediment (Aarhus Bay, Denmark): abundance and diversity related to geochemical zonation[J]. Environmental Microbiology, 2009, 11(5): 1278-1291. DOI PMID
[69]	MA L, SHE W Y, WU G, et al. Influence of temperature and sulfate concentration on the sulfate/sulfite reduction prokaryotic communities in the Tibetan hot springs[J]. Microorganisms, 2021, 9(3): 583. DOI URL
[70]	MORI K, KIM H, KAKEGAWA T, et al. A novel lineage of sulfate-reducing microorganisms: Thermodesulfobiaceae fam. nov., Thermodesulfobium narugense, gen. nov., sp nov., a new thermophilic isolate from a hot spring[J]. Extremophiles, 2003, 7(4): 283-290. DOI URL
[71]	STETTER K O, LAUERER G, THOMM M, et al. Isolation of extremely thermophilic sulfate reducers: evidence for a novel branch of archaebacteria[J]. Science, 1987, 236(4803): 822-824. PMID
[72]	ITOH T, SUZUKI K, SANCHEZ P C, et al. Caldivirga maquilingensis gen. nov., sp nov., a new genus of rod-shaped crenarchaeote isolated from a hot spring in the Philippines[J]. International Journal of Systematic Bacteriology, 1999, 49(3): 1157-1163.
[73]	SIEBERS B, ZAPARTY M, RADDATZ G, et al. The complete genome sequence of Thermoproteus tenax: a physiologically versatile member of the Crenarchaeota[J]. PLoS One, 2011, 6(10): e24222. DOI URL
[74]	CHERNYH N A, NEUKIRCHEN S, FROLOV E N, et al. Dissimilatory sulfate reduction in the archaeon ‘Candidatus Vulcanisaeta moutnovskia’ sheds light on the evolution of sulfur metabolism[J]. Nature Microbiology, 2020, 5(11): 1428-1438. DOI URL
[75]	DAVID L A, ALM E J. Rapid evolutionary innovation during an Archaean genetic expansion[J]. Nature, 2011, 469(7328): 93-96. DOI URL
[76]	ZHOU J Z, HE Q, HEMME C L, et al. How sulphate-reducing microorganisms cope with stress: lessons from systems biology[J]. Nature Reviews Microbiology, 2011, 9(6): 452-466. DOI PMID
[77]	SHEN Y N, BUICK R. The antiquity of microbial sulfate reduction[J]. Earth-Science Reviews, 2004, 64(3/4): 243-272. DOI URL
[78]	UENO Y, ONO S, RUMBLE D, et al. Quadruple sulfur isotope analysis of Ca. 3.5 Ga Dresser Formation: new evidence for microbial sulfate reduction in the early Archean[J]. Geochimica et Cosmochimica Acta, 2008, 72(23): 5675-5691. DOI URL
[79]	SHEN Y N, FARQUHAR J, MASTERSON A, et al. Evaluating the role of microbial sulfate reduction in the early Archean using quadruple isotope systematics[J]. Earth and Planetary Science Letters, 2009, 279(3/4): 383-391. DOI URL
[80]	JEANTHON C, L’HARIDON S, CUEFF V, et al. Thermodesulfobacterium hydrogeniphilum sp. nov., a thermophilic, chemolithoautotrophic, sulfate-reducing bacterium isolated from a deep-sea hydrothermal vent at Guaymas Basin, and emendation of the genus Thermodesulfobacterium[J]. International Journal of Systematic and Evolutionary Microbiology, 2002, 52(3): 765-772.
[81]	MOUSSARD H, L’HARIDON S, TINDALL B J, et al. Thermodesulfatator indicus gen. nov., sp. nov., a novel thermophilic chemolithoautotrophic sulfate-reducing bacterium isolated from the Central Indian Ridge[J]. International Journal of Systematic and Evolutionary Microbiology, 2004, 54(1): 227-233. DOI URL
[82]	SEKIGUCHI Y, MURAMATSU M, IMACHI H, et al. Thermodesulfovibrio aggregans sp. nov. and Thermodesulfovibrio thiophilus sp. nov., anaerobic, thermophilic, sulfate-reducing bacteria isolated from thermophilic methanogenic sludge, and emended description of the genus Thermodesulfovibrio[J]. International journal of systematic and evolutionary microbiology, 2008, 58(11): 2541-2548. DOI URL
[83]	SIEVERT S M, KUEVER J. Desulfacinum hydrothermale sp. nov., a thermophilic, sulfate-reducing bacterium from geothermally heated sediments near Milos Island (Greece)[J]. International Journal of Systematic and Evolutionary Microbiology, 2000, 50(3): 1239-1246. DOI URL
[84]	VIGNERON A, CRUAUD P, CULLEY A I, et al. Genomic evidence for sulfur intermediates as new biogeochemical hubs in a model aquatic microbial ecosystem[J]. Microbiome, 2021, 9(1): 46. DOI PMID
[85]	ANANTHARAMAN K, HAUSMANN B, JUNGBLUTH S P, et al. Expanded diversity of microbial groups that shape the dissimilatory sulfur cycle[J]. The ISME Journal, 2018, 12(7): 1715-1728. DOI URL
[86]	ZHANG J Z, MILLERO F J. The rate of sulfite oxidation in seawater[J]. Geochimica et Cosmochimica Acta, 1991, 55(3): 677-685. DOI URL
[87]	FINSTER K. Microbiological disproportionation of inorganic sulfur compounds[J]. Journal of Sulfur Chemistry, 2008, 29(3/4): 281-292. DOI URL
[88]	ZINDER S, BROCK T D. Sulfur dioxide in geothermal waters and gases[J]. Geochimica et Cosmochimica Acta, 1977, 41(1): 73-79. DOI URL
[89]	COLMAN D R, LINDSAY M R, AMENABAR M J, et al. Phylogenomic analysis of novel Diaforarchaea is consistent with sulfite but not sulfate reduction in volcanic environments on early Earth[J]. The ISME Journal, 2020, 14(5): 1316-1331. DOI URL
[90]	WACEY D, KILBURN M R, SAUNDERS M, et al. Microfossils of sulphur-metabolizing cells in 3.4-billion-year-old rocks of Western Australia[J]. Nature Geoscience, 2011, 4(10): 698-702. DOI URL
[91]	PHILIPPOT P, VAN ZUILEN M V, LEPOT K, et al. Early Archaean microorganisms preferred elemental sulfur, not sulfate[J]. Science, 2007, 317(5844): 1534-1537. PMID
[92]	FINSTER K W, KJELDSEN K U, KUBE M, et al. Complete genome sequence of Desulfocapsa sulfexigens, a marine deltaproteobacterium specialized in disproportionating inorganic sulfur compounds[J]. Standards in Genomic Sciences, 2013, 8(1): 58-68. DOI URL
[93]	MARDANOV A V, BELETSKY A V, KADNIKOV V V, et al. Genome analysis of thermosulfurimonas dismutans, the first thermophilic sulfur-disproportionating bacterium of the phylum thermodesulfobacteria[J]. Frontiers in Microbiology, 2016, 7: 950.
[94]	SLOBODKIN A, REYSENBACH A L, SLOBODKINA G B, et al. Dissulfuribacter thermophilus gen. nov., sp. nov., a thermophilic, autotrophic, sulfur-disproportionating, deeply branching deltaproteobacterium from a deep-sea hydrothermal vent[J]. International Journal of Systematic and Evolutionary Microbiology, 2013, 63(6): 1967-1971. DOI URL
[95]	SLOBODKIN A I, SLOBODKINA G B, PANTELEEVA A, et al. Dissulfurimicrobium hydrothermale gen. nov., sp. nov., a thermophilic, autotrophic, sulfur-disproportionating deltaproteobacterium isolated from a hydrothermal pond[J]. International Journal of Systematic and Evolutionary Microbiology, 2016, 66(2): 1022-1026. DOI URL
[96]	KOJIMA H, UMEZAWA K, FUKUI M. Caldimicrobium thiodismutans sp. nov., a sulfur-disproportionating bacterium isolated from a hot spring, and emended description of the genus Caldimicrobium[J]. International Journal of Systematic and Evolutionary Microbiology, 2016, 66(4): 1828-1831. DOI URL
[97]	CZAJA A D, JOHNSON C M, BEARD B L, et al. Biological Fe oxidation controlled deposition of banded iron formation in the Ca. 3770 Ma Isua Supracrustal Belt (West Greenland)[J]. Earth and Planetary Science Letters, 2013, 363: 192-203. DOI URL
[98]	LI W Q, CZAJA A D, VAN KRANENDONK M J, et al. An anoxic, Fe(II)-rich, U-poor ocean 3.46 billion years ago[J]. Geochimica et Cosmochimica Acta, 2013, 120: 65-79. DOI URL
[99]	TICE M M, LOWE D R. Photosynthetic microbial mats in the 3, 416-myr-old ocean[J]. Nature, 2004, 431(7008): 549-552. DOI URL
[100]	WESTALL F, DE RONDE C E J, SOUTHAM G, et al. Implications of a 3.472-3.333 Gyr-old subaerial microbial mat from the Barberton greenstone belt, South Africa for the UV environmental conditions on the early Earth[J]. Philosophical Transactions of the Royal Society B: Biological Sciences, 2006, 361(1474): 1857-1875. DOI URL
[101]	BONTOGNALI T R R, SESSIONS A L, ALLWOOD A C, et al. Sulfur isotopes of organic matter preserved in 3.45-billion-year-old stromatolites reveal microbial metabolism[J]. Proceedings of the National Academy of Sciences of the United States of America, 2012, 109(38): 15146-15151. PMID
[102]	MCLOUGHLIN N, GROSCH E, KILBURN M, et al. Sulfur isotope evidence for a paleoarchean subseafloor biosphere, Barberton, South Africa[J]. Geology, 2012, 40(11): 1031-1034. DOI URL
[103]	GRASSINEAU N V, ABELL P, APPEL P W U, et al. Early life signatures in sulfur and carbon isotopes from Isua, Barberton, Wabigoon (Steep Rock), and Belingwe Greenstone Belts (3.8 to 2.7 Ga)[M]//KESLER S E, OHMOTO H. Evolution of early Earth’s atmosphere, hydrosphere, and biosphere:Constraints from ore deposits. Colorado: Geological Society of America, 2006: 33-52.
[104]	MULLER É, PHILIPPOT P, ROLLION-BARD C, et al. Primary sulfur isotope signatures preserved in high-grade Archean barite deposits of the Sargur Group, Dharwar Craton, India[J]. Precambrian Research, 2017, 295: 38-47. DOI URL
[105]	UENO Y, YAMADA K, YOSHIDA N, et al. Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era[J]. Nature, 2006, 440(7083): 516-519. DOI URL
[106]	STÜEKEN E E, BUICK R. Environmental control on microbial diversification and methane production in the Mesoarchean[J]. Precambrian Research, 2018, 304: 64-72. DOI URL
[107]	BUICK R, DUNLOP J S R. Evaporitic sediments of early Archaean age from the Warrawoona Group, North Pole, Western Australia[J]. Sedimentology, 1990, 37(2): 247-277. DOI URL
[108]	FLANNERY D T, ALLWOOD A C, SUMMONS R E, et al. Spatially-resolved isotopic study of carbon trapped in -3.43 Ga Strelley Pool Formation stromatolites[J]. Geochimica et Cosmochimica Acta, 2018, 223: 21-35. DOI URL
[109]	RYE R, HOLLAND H D. Life associated with a 2.76 Ga ephemeral pond: evidence from Mount Roe#2 paleosol[J]. Geology, 2000, 28(6): 483-486. DOI URL
[110]	YOSHIYA K, NISHIZAWA M, SAWAKI Y, et al. In situ iron isotope analyses of pyrite and organic carbon isotope ratios in the Fortescue Group: metabolic variations of a Late Archean ecosystem[J]. Precambrian Research, 2012, 212/213: 169-193. DOI URL
[111]	YOSHIYA K, SAWAKI Y, SHIBUYA T, et al. In-situ iron isotope analyses of pyrites from 3.5 to 3.2 Ga sedimentary rocks of the Barberton Greenstone Belt, Kaapvaal Craton[J]. Chemical Geology, 2015, 403: 58-73. DOI URL
[112]	STÜEKEN E E, BUICK R, GUY B M, et al. Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr[J]. Nature, 2015, 520(7549): 666-669. DOI URL
[113]	GARVIN J, BUICK R, ANBAR A D, et al. Isotopic evidence for an aerobic nitrogen cycle in the latest Archean[J]. Science, 2009, 323(5917): 1045-1048. DOI PMID
[114]	THOMAZO C, PINTI D L, BUSIGNY V, et al. Biological activity and the Earth’s surface evolution: insights from carbon, sulfur, nitrogen and iron stable isotopes in the rock record[J]. Comptes Rendus Palevol, 2009, 8(7): 665-678. DOI URL
[115]	CRADDOCK P R, DAUPHAS N. Iron and carbon isotope evidence for microbial iron respiration throughout the Archean[J]. Earth and Planetary Science Letters, 2011, 303(1/2): 121-132. DOI URL
[116]	CROWE S A, JONES C, KATSEV S, et al. Photoferrotrophs thrive in an Archean Ocean analogue[J]. Proceedings of the National Academy of Sciences of the United States of America, 2008, 105(41): 15938-15943. DOI PMID
[117]	HEARD A W, DAUPHAS N, GUILBAUD R, et al. Triple iron isotope constraints on the role of ocean iron sinks in early atmospheric oxygenation[J]. Science, 2020, 370(6515): 446-449. DOI PMID
[118]	KUMP L R, BARLEY M E. Increased subaerial volcanism and the rise of atmospheric oxygen 2.5 billion years ago[J]. Nature, 2007, 448(7157): 1033-1036. DOI URL
[119]	HOLM N G. The ¹³C/¹²C ratios of siderite and organic matter of a modern metalliferous hydrothermal sediment and their implications for banded iron formations[J]. Chemical Geology, 1989, 77(1): 41-45. DOI URL
[120]	BRATERMAN P S, CAIRNS-SMITH A G, SLOPER R W. Photo-oxidation of hydrated Fe²⁺: significance for banded iron formations[J]. Nature, 1983, 303(5913): 163-164. DOI URL
[121]	WIDDEL F, SCHNELL S, HEISING S, et al. Ferrous iron oxidation by anoxygenic phototrophic bacteria[J]. Nature, 1993, 362(6423): 834-836. DOI URL
[122]	HEGLER F, POSTH N R, JIANG J, et al. Physiology of phototrophic iron(II)-oxidizing bacteria: implications for modern and ancient environments[J]. FEMS Microbiology Ecology, 2008, 66(2): 250-260. DOI PMID
[123]	WU W F, SWANNER E D, HAO L K, et al. Characterization of the physiology and cell-mineral interactions of the marine anoxygenic phototrophic Fe(II) oxidizer Rhodovulum iodosum: implications for Precambrian Fe(II) oxidation[J]. FEMS Microbiology Ecology, 2014, 88(3): 503-515. DOI URL
[124]	HEISING S, RICHTER L, LUDWIG W, et al. Chlorobium ferrooxidans sp. nov., a phototrophic green sulfur bacterium that oxidizes ferrous iron in coculture with a “Geospirillum” sp. strain[J]. Archives of Microbiology, 1999, 172(2): 116-124. DOI URL
[125]	RICKARD D, LUTHER G W. Chemistry of iron sulfides[J]. Chemical Reviews, 2007, 107(2): 514-562. PMID
[126]	BERG J S, DUVERGER A, CORDIER L, et al. Rapid pyritization in the presence of a sulfur/sulfate-reducing bacterial consortium[J]. Scientific Reports, 2020, 10(1): 8264. DOI PMID
[127]	FRANK K L, ROGERS K L, ROGERS D R, et al. Key factors influencing rates of heterotrophic sulfate reduction in active seafloor hydrothermal massive sulfide deposits[J]. Frontiers in Microbiology, 2015, 6: 1449. DOI PMID
[128]	FRANK K L, ROGERS D R, OLINS H C, et al. Characterizing the distribution and rates of microbial sulfate reduction at Middle Valley hydrothermal vents[J]. The ISME Journal, 2013, 7(7): 1391-1401. DOI URL
[129]	DILLON J G, FISHBAIN S, MILLER S R, et al. High rates of sulfate reduction in a low-sulfate hot spring microbial mat are driven by a low level of diversity of sulfate-respiring microorganisms[J]. Applied and Environmental Microbiology, 2007, 73(16): 5218-5226. PMID
[130]	CANFIELD D E, HABICHT K S, THAMDRUP B. The Archean sulfur cycle and the early history of atmospheric oxygen[J]. Science, 2000, 288(5466): 658-661. PMID
[131]	MA L, WU G, YANG J, et al. Distribution of hydrogen-producing bacteria in Tibetan hot springs, China[J]. Frontiers in Microbiology, 2021, 12: 569020. DOI URL
[132]	RABUS R, VENCESLAU S S, WÖHLBRAND L, et al. A post-genomic view of the ecophysiology, catabolism and biotechnological relevance of sulphate-reducing prokaryotes[J]. Advances in Microbial Physiology, 2015, 66: 55-321. DOI PMID
[133]	LYONS T W, REINHARD C T, PLANAVSKY N J. The rise of oxygen in Earth’s early ocean and atmosphere[J]. Nature, 2014, 506(7488): 307-315. DOI URL
[134]	SIPMA J, LETTINGA G, STAMS A J M, et al. Hydrogenogenic CO conversion in a moderately thermophilic (55 ℃) sulfate-fed gas lift reactor: competition for CO-derived H₂[J]. Biotechnology Progress, 2006, 22(5): 1327-1334. DOI URL
[135]	VAN HOUTEN R T, YUN S Y, LETTINGA G. Thermophilic sulphate and sulphite reduction in lab-scale gas-lift reactors using H₂ and CO₂ as energy and carbon source[J]. Biotechnology and Bioengineering, 1997, 55(5): 807-814. DOI URL
[136]	BEAL E, CLAIRE M, HOUSE C. High rates of anaerobic methanotrophy at low sulfate concentrations with implications for past and present methane levels[J]. Geobiology, 2011, 9(2): 131-139. DOI PMID
[137]	KALLMEYER J, BOETIUS A. Effects of temperature and pressure on sulfate reduction and anaerobic oxidation of methane in hydrothermal sediments of Guaymas Basin[J]. Applied and Environmental Microbiology, 2004, 70(2): 1231-1233. DOI PMID
[138]	MCKAY L J, DLAKIĆ M, FIELDS M W, et al. Co-occurring genomic capacity for anaerobic methane and dissimilatory sulfur metabolisms discovered in the Korarchaeota[J]. Nature Microbiology, 2019, 4(4): 614-622. DOI PMID
[139]	GODFREY L V, FALKOWSKI P G. The cycling and redox state of nitrogen in the Archaean Ocean[J]. Nature Geoscience, 2009, 2(10): 725-729. DOI URL
[140]	STÜEKEN E E, KIPP M A, KOEHLER M C, et al. The evolution of Earth’s biogeochemical nitrogen cycle[J]. Earth-Science Reviews, 2016, 160: 220-239. DOI URL
[141]	SHAO M F, ZHANG T, FANG H H P. Sulfur-driven autotrophic denitrification: diversity, biochemistry, and engineering applications[J]. Applied Microbiology and Biotechnology, 2010, 88(5): 1027-1042. DOI URL
[142]	JIAO J Y, LIAN Z H, LI M M, et al. Comparative genomic analysis of Thermus provides insights into the evolutionary history of an incomplete denitrification pathway[J]. mLife, 2022, 2: 198-209.
[143]	SKIRNISDOTTIR S, HREGGVIDSSON G O, HOLST O, et al. Isolation and characterization of a mixotrophic sulfur-oxidizing Thermus scotoductus[J]. Extremophiles, 2001, 5(1): 45-51. DOI URL
[144]	AMEND J P, ROGERS K L, SHOCK E L, et al. Energetics of chemolithoautotrophy in the hydrothermal system of Vulcano Island, southern Italy[J]. Geobiology, 2003, 1(1): 37-58. DOI URL
[145]	LI G X, LI H, XIAO K Q, et al. Thiosulfate reduction coupled with anaerobic ammonium oxidation by Ralstonia sp. GX3-BWBA[J]. ACS Earth and Space Chemistry, 2020, 4(12): 2426-2434. DOI URL
[146]	LI Y F, TANG K, ZHANG L B, et al. Coupled carbon, sulfur, and nitrogen cycles mediated by microorganisms in the water column of a shallow-water hydrothermal ecosystem[J]. Frontiers in Microbiology, 2018, 9: 2718. DOI PMID

太古宙样本	分馏结果	年龄/Ga	推测过程	文献
Isua Supracrustal Belt BIFs, West Greenland	δ⁵⁶Fe=0.4‰~1.1‰	3.7	Anoxygenic Photosynthesis	[97]
Marble Bar Chert, Australia	δ⁵⁶Fe=1.5‰~2.6‰	3.46	Anoxygenic Photosynthesis	[98]
Buck Reef Chert, South Africa	δ¹³C=-35‰~-20‰	3.42	Anoxygenic Photosynthesis	[99]
Barberton Greenstone Belt, South Africa	δ¹³C=-26.8‰~-22.7‰	3.47	Anoxygenic Photosynthesis	[100]
Strelley Pool Formation, Australia	δ³⁴S=-40‰~25‰	3.45	Sulfur Metabolism	[101]
Barberton Greenstone Belt, South Africa	δ³⁴S=-39.8‰~-3.2‰	3.45	Sulfur Metabolism	[102]
Isua Greenstone Belt, West Greenland	δ³⁴S=-3.8‰~3.4‰	3.8	Sulfur Metabolism	[103]
Dresser Formation, Western Australia	δ³⁴S=-22‰~-14‰	3.5	Sulfate Reduction	[78]
Sargur Group, India	δ³⁴S=-11.4‰~-8.3‰	3.2	Sulfate Reduction	[104]
Pyrites Within Barites, Pilbara Craton	δ³⁴S/δ³²S=25‰	3.47	Sulfate Reduction	[79]
Dresser Formation, Western Australia	Δ³³S=2.3‰±1.8‰	3.49	Sulfur Disproportionation	[91]
Microscopic pyrite, Strelley Pool Formation, Australia	Δ³³S=-1.7‰±1.4‰	3.45	Sulfur Disproportionation	[90]
Dresser Formation, Western Australia	δ¹³C=-56‰	3.47	Methanogenesis	[105]
Lalla Rookh Sandstone, Western Australia	δ¹³C=-38‰~-30‰	3.0	Methanogenesis	[106]
Fortesque Group, Tumbiana Formation	δ¹³C=-50‰~-40‰	2.72	Methanogenesis	[107]
Strelley Pool Formation stromatolites, Australia	δ¹³C=-45‰~-29‰	3.43	Methanotrophy	[108]
Mount Roe Paleosol, Western Australia	δ¹³C=-51‰~-33‰	2.77	Methanotrophy	[109]
Fortescue Group, Australia	δ⁵⁶Fe=-4.2‰~3.0‰	2.7	Iron Reduction	[110]
Barberton Greenstone Belt, Kaapvaal Craton	δ⁵⁶Fe=-1.8‰~3.8‰	3.2	Iron Reduction	[111]
Marine and fluvial sedimentary rocks	δ¹⁵N=0±1.2‰	3.2	Nitrogen Fixation	[112]
Mount McRae, Australia	δ¹⁵N=1‰~7.5‰	2.5	Nitrification/Denitrification	[113]

太古宙样本	分馏结果	年龄/Ga	推测过程	文献
Isua Supracrustal Belt BIFs, West Greenland	δ⁵⁶Fe=0.4‰~1.1‰	3.7	Anoxygenic Photosynthesis	[97]
Marble Bar Chert, Australia	δ⁵⁶Fe=1.5‰~2.6‰	3.46	Anoxygenic Photosynthesis	[98]
Buck Reef Chert, South Africa	δ¹³C=-35‰~-20‰	3.42	Anoxygenic Photosynthesis	[99]
Barberton Greenstone Belt, South Africa	δ¹³C=-26.8‰~-22.7‰	3.47	Anoxygenic Photosynthesis	[100]
Strelley Pool Formation, Australia	δ³⁴S=-40‰~25‰	3.45	Sulfur Metabolism	[101]
Barberton Greenstone Belt, South Africa	δ³⁴S=-39.8‰~-3.2‰	3.45	Sulfur Metabolism	[102]
Isua Greenstone Belt, West Greenland	δ³⁴S=-3.8‰~3.4‰	3.8	Sulfur Metabolism	[103]
Dresser Formation, Western Australia	δ³⁴S=-22‰~-14‰	3.5	Sulfate Reduction	[78]
Sargur Group, India	δ³⁴S=-11.4‰~-8.3‰	3.2	Sulfate Reduction	[104]
Pyrites Within Barites, Pilbara Craton	δ³⁴S/δ³²S=25‰	3.47	Sulfate Reduction	[79]
Dresser Formation, Western Australia	Δ³³S=2.3‰±1.8‰	3.49	Sulfur Disproportionation	[91]
Microscopic pyrite, Strelley Pool Formation, Australia	Δ³³S=-1.7‰±1.4‰	3.45	Sulfur Disproportionation	[90]
Dresser Formation, Western Australia	δ¹³C=-56‰	3.47	Methanogenesis	[105]
Lalla Rookh Sandstone, Western Australia	δ¹³C=-38‰~-30‰	3.0	Methanogenesis	[106]
Fortesque Group, Tumbiana Formation	δ¹³C=-50‰~-40‰	2.72	Methanogenesis	[107]
Strelley Pool Formation stromatolites, Australia	δ¹³C=-45‰~-29‰	3.43	Methanotrophy	[108]
Mount Roe Paleosol, Western Australia	δ¹³C=-51‰~-33‰	2.77	Methanotrophy	[109]
Fortescue Group, Australia	δ⁵⁶Fe=-4.2‰~3.0‰	2.7	Iron Reduction	[110]
Barberton Greenstone Belt, Kaapvaal Craton	δ⁵⁶Fe=-1.8‰~3.8‰	3.2	Iron Reduction	[111]
Marine and fluvial sedimentary rocks	δ¹⁵N=0±1.2‰	3.2	Nitrogen Fixation	[112]
Mount McRae, Australia	δ¹⁵N=1‰~7.5‰	2.5	Nitrification/Denitrification	[113]