Research progress and prospects of metal-dependent anaerobic methane oxidation in marine sediments

XIN Youzhi; SUN Zhilei; WANG Hongmei; CHEN Ye; XU Cuiling; GENG Wei; CAO Hong; ZHANG Xilin; ZHANG Xianrong; LI Xin; YAN Dawei; WU Nengyou

doi:10.16562/j.cnki.0256-1492.2020122801

2021 Vol. 41, No. 5

Article Contents

Article navigation > Marine Geology & Quaternary Geology > 2021 > 41(5): 58-66

Next Article Previous Article

XIN Youzhi, SUN Zhilei, WANG Hongmei, CHEN Ye, XU Cuiling, GENG Wei, CAO Hong, ZHANG Xilin, ZHANG Xianrong, LI Xin, YAN Dawei, WU Nengyou. Research progress and prospects of metal-dependent anaerobic methane oxidation in marine sediments[J]. Marine Geology & Quaternary Geology, 2021, 41(5): 58-66. doi: 10.16562/j.cnki.0256-1492.2020122801

Citation:

XIN Youzhi, SUN Zhilei, WANG Hongmei, CHEN Ye, XU Cuiling, GENG Wei, CAO Hong, ZHANG Xilin, ZHANG Xianrong, LI Xin, YAN Dawei, WU Nengyou. Research progress and prospects of metal-dependent anaerobic methane oxidation in marine sediments[J]. Marine Geology & Quaternary Geology, 2021, 41(5): 58-66. doi: 10.16562/j.cnki.0256-1492.2020122801

Research progress and prospects of metal-dependent anaerobic methane oxidation in marine sediments

1.
School of Earth Sciences, China University of Geosciences, Wuhan 430074, China
2.
Key Laboratory of Gas Hydrate, Ministry of Natural Resources, Qingdao Institute of Marine Geology, Qingdao 266237, China
3.
Laboratory for Marine Mineral Resources, Pilot National Laboratory for Marine Science and Technology, Qingdao 266237, China
4.
State Key Laboratory of Biogeology and Environmental Geology, China University of Geosciences, Wuhan 430074, China

More Information

Corresponding authors: WANG Hongmei, wanghmei04@163.com ; WU Nengyou, wuny@ms.giec.ac.cn

Received Date: 28 December 2020

Revised Date: 03 March 2021

Publish Date: 28 October 2021

Abstract

Abstract

A large fraction of methane is consumed by anaerobic oxidation (AOM) in marine sediments. Previous researches suggested that AOM is coupled to the reduction of sulfate, nitrate and nitrite, which may effectively reduce methane emission into the atmosphere. Recently, metal-dependent AOM (metal-AOM, AOM driven by active metal oxides reduction reaction) was demonstrated to occur in both the sediments in nature and enriched cultures. But the elusive microorganisms mediating metal-AOM process have not yet been isolated from natural marine environments, and most researches on metal-AOM in marine sediments focus on special marine habitats such as hydrothermal vents or cold seeps. However, a series of investigation shows that geological fluids play an important role in the maintenance and evolution of these submarine chemolithoautotrophy ecosystems, and profoundly affect the global geochemical cycle. Therefore, the research on this scientific problem has attracted more and more attention from marine scientists. In this review, the potential microbial communities and geochemical evidence of metal-AOM in marine sediments are summarized. On the basis of literature researches, taking the cold seeps and hydrothermal vents coexisted region, the Okinawa Trough, as an example, a new metal-AOM mechanism is proposed. The investigation in the global cold seeps and hydrothermal vents system interaction areas could be beneficial to better discuss the mechanism of metal-AOM and the connectivity of microbial distribution in deep-sea habitats.
- marine sediments /
- metal-dependent anaerobic oxidation of methane /
- cold seeps and hydrothermal vents coexisted region /
- Okinawa Trough

FullText(HTML)

References

[1]	Moran M A. The global ocean microbiome [J]. Science, 2015, 350(6266): aac8455. doi: 10.1126/science.aac8455 CrossRef Google Scholar
[2]	D’Hondt S, Pockalny R, Fulfer V M, et al. Subseaﬂoor life and its biogeochemical impacts [J]. Nature Communication, 2019, 10(1): 3519. doi: 10.1038/s41467-019-11450-z CrossRef Google Scholar
[3]	Parkes R J, Cragg B A, Bale S J, et al. Deep bacterial biosphere in Pacific Ocean sediments [J]. Nature, 1994, 371(6496): 410-413. doi: 10.1038/371410a0 CrossRef Google Scholar
[4]	孙治雷, 魏合龙, 王利波, 等. 海底冷泉系统的碳循环问题及探测[J]. 应用海洋学学报, 2016, 35(3):442-450 doi: 10.3969/J.ISSN.2095-4972.2016.03.017 CrossRef Google Scholar SUN Zhilei, WEI Helong, WANG Libo, et al. Focus issues of carbon cycle and detecting technologies in seafloor cold seepages [J]. Journal of Applied Oceanography, 2016, 35(3): 442-450. doi: 10.3969/J.ISSN.2095-4972.2016.03.017 CrossRef Google Scholar
[5]	Hutchins D A, Fu F X. Microorganisms and ocean global change [J]. Nature Microbiology, 2017, 2: 17058. doi: 10.1038/nmicrobiol.2017.58 CrossRef Google Scholar
[6]	Iversen N, Jørgensen B B. Anaerobic methane oxidation rates at the sulfate-methane transition in marine sediments from Kattegat and Skagerrak (Denmark) [J]. Limnology and Oceanography, 1985, 30(5): 944-955. doi: 10.4319/lo.1985.30.5.0944 CrossRef Google Scholar
[7]	Timmers PHA, Welte CU, Koehorst JJ, et al. Reverse methanogenesis and respiration in methanotrophic archaea [J]. Archaea, 2017, 2017: 1654237. Google Scholar
[8]	Norði K Á, Thamdrup B. Nitrate-dependent anaerobic methane oxidation in a freshwater sediment [J]. Geochimica et Cosmochimica Acta, 2014, 132: 141-150. doi: 10.1016/j.gca.2014.01.032 CrossRef Google Scholar
[9]	Shen L D, Hu B L, Liu S, et al. Anaerobic methane oxidation coupled to nitrite reduction can be a potential methane sink in coastal environments [J]. Applied Microbiology and Biotechnology, 2016, 100(16): 7171-7180. doi: 10.1007/s00253-016-7627-0 CrossRef Google Scholar
[10]	Zehnder A J B, Brock T D. Anaerobic methane oxidation: occurrence and ecology [J]. Applied and Environmental Microbiology, 1980, 39(1): 194-204. doi: 10.1128/AEM.39.1.194-204.1980 CrossRef Google Scholar
[11]	Bau M, Dulski P. Distribution of yttrium and rare-earth elements in the Penge and Kuruman iron-formations, Transvaal Supergroup, South Africa [J]. Precambrian Research, 1996, 79(1-2): 37-55. doi: 10.1016/0301-9268(95)00087-9 CrossRef Google Scholar
[12]	He Z F, Zhang Q Y, Feng Y D, et al. Microbiological and environmental significance of metal-dependent anaerobic oxidation of methane [J]. Science of the Total Environment, 2018, 610-611: 759-768. doi: 10.1016/j.scitotenv.2017.08.140 CrossRef Google Scholar
[13]	Kvenvolden K A, Rogers B W. Gaia’s breath—global methane exhalations [J]. Marine and Petroleum Geology, 2005, 22(4): 579-590. doi: 10.1016/j.marpetgeo.2004.08.004 CrossRef Google Scholar
[14]	Hoehler T M, Alperin M J, Albert D B, et al. Field and laboratory studies of methane oxidation in an anoxic marine sediment: evidence for a methanogen-sulfate reducer consortium [J]. Global Biogeochemical Cycles, 1994, 8(4): 451-463. doi: 10.1029/94GB01800 CrossRef Google Scholar
[15]	Hinrichs K U, Hayes J M, Sylva S P, et al. Methane-consuming archaebacteria in marine sediments [J]. Nature, 1999, 398(6730): 802-805. doi: 10.1038/19751 CrossRef Google Scholar
[16]	Knittel K, Lösekann T, Boetius A, et al. Diversity and distribution of methanotrophic archaea at cold seeps [J]. Applied and Environmental Microbiology, 2005, 71(1): 467-479. doi: 10.1128/AEM.71.1.467-479.2005 CrossRef Google Scholar
[17]	Brazelton W J, Schrenk M O, Kelley D S, et al. Methane- and sulfur-metabolizing microbial communities dominate the lost city hydrothermal field ecosystem [J]. Applied and Environmental Microbiology, 2006, 72(9): 6257-6270. doi: 10.1128/AEM.00574-06 CrossRef Google Scholar
[18]	D'Hondt S, Rutherford S, Spivack A J. Metabolic activity of subsurface life in deep-sea sediments [J]. Science, 2002, 295(5562): 2067-2070. doi: 10.1126/science.1064878 CrossRef Google Scholar
[19]	Bowles M W, Samarkin V A, Bowles K M, et al. Weak coupling between sulfate reduction and the anaerobic oxidation of methane in methane-rich seafloor sediments during ex situ incubation [J]. Geochimica et Cosmochimica Acta, 2011, 75(2): 500-519. doi: 10.1016/j.gca.2010.09.043 CrossRef Google Scholar
[20]	Wankel S D, Adams M M, Johnston D T, et al. Anaerobic methane oxidation in metalliferous hydrothermal sediments: influence on carbon flux and decoupling from sulfate reduction [J]. Environmental Microbiology, 2012, 14(10): 2726-2740. doi: 10.1111/j.1462-2920.2012.02825.x CrossRef Google Scholar
[21]	Sivan O, Adler M, Pearson A, et al. Geochemical evidence for iron-mediated anaerobic oxidation of methane [J]. Limnology and Oceanography, 2011, 56(4): 1536-1544. doi: 10.4319/lo.2011.56.4.1536 CrossRef Google Scholar
[22]	Ettwig K F, Butler M K, Le Paslier D, et al. Nitrite-driven anaerobic methane oxidation by oxygenic bacteria [J]. Nature, 2010, 464(7288): 543-548. doi: 10.1038/nature08883 CrossRef Google Scholar
[23]	Crowe S A, Katsev S, Leslie K, et al. The methane cycle in ferruginous Lake Matano [J]. Geobiology, 2011, 9(1): 61-78. doi: 10.1111/j.1472-4669.2010.00257.x CrossRef Google Scholar
[24]	Norði K Á, Thamdrup B, Schubert C J. Anaerobic oxidation of methane in an iron-rich Danish freshwater lake sediment [J]. Limnology and Oceanography, 2013, 58(2): 546-554. doi: 10.4319/lo.2013.58.2.0546 CrossRef Google Scholar
[25]	Riedinger N, Formolo M J, Lyons T W, et al. An inorganic geochemical argument for coupled anaerobic oxidation of methane and iron reduction in marine sediments [J]. Geobiology, 2014, 12(2): 172-181. doi: 10.1111/gbi.12077 CrossRef Google Scholar
[26]	Raghoebarsing A A, Pol A, Van De Pas-Schoonen K, et al. A microbial consortium couples anaerobic methane oxidation to denitrification [J]. Nature, 2006, 440(7086): 918-921. doi: 10.1038/nature04617 CrossRef Google Scholar
[27]	Bar-Or I, Elvert M, Eckert W, et al. Iron-coupled anaerobic oxidation of methane performed by a mixed bacterial-archaeal community based on poorly reactive minerals [J]. Environmental Science & Technology, 2017, 51(21): 12293-12301. Google Scholar
[28]	Knittel K, Boetius A. Anaerobic oxidation of methane: progress with an unknown process [J]. Annual Review of Microbiology, 2009, 63: 311-334. doi: 10.1146/annurev.micro.61.080706.093130 CrossRef Google Scholar
[29]	Haroon M F, Hu S H, Shi Y, et al. Anaerobic oxidation of methane coupled to nitrate reduction in a novel archaeal lineage [J]. Nature, 2013, 500(7464): 567-570. doi: 10.1038/nature12375 CrossRef Google Scholar
[30]	Hu S H, Zeng R J, Burow L C, et al. Enrichment of denitrifying anaerobic methane oxidizing microorganisms [J]. Environmental Microbiology Reports, 2009, 1(5): 377-384. doi: 10.1111/j.1758-2229.2009.00083.x CrossRef Google Scholar
[31]	Ettwig K F, Zhu B L, Speth D, et al. Archaea catalyze iron-dependent anaerobic oxidation of methane [J]. Proceedings of the National Academy of Sciences of the United States of America, 2016, 113(45): 12792-12796. doi: 10.1073/pnas.1609534113 CrossRef Google Scholar
[32]	Cai C, Leu A O, Xie G J, et al. A methanotrophic archaeon couples anaerobic oxidation of methane to Fe (III) reduction [J]. The ISME Journal, 2018, 12(8): 1929-1939. doi: 10.1038/s41396-018-0109-x CrossRef Google Scholar
[33]	Weber H S, Habicht K S, Thamdrup B. Anaerobic methanotrophic archaea of the ANME-2d cluster are active in a low-sulfate, iron-rich freshwater sediment [J]. Frontiers in Microbiology, 2017, 8: 619. Google Scholar
[34]	Niu M Y, Fan X B, Zhuang G C, et al. Methane-metabolizing microbial communities in sediments of the Haima cold seep area, northwest slope of the South China Sea [J]. FEMS Microbiology Ecology, 2017, 93(9): fix101. Google Scholar
[35]	Beal E J, House C H, Orphan V J. Manganese- and iron-dependent marine methane oxidation [J]. Science, 2009, 325(5937): 184-187. doi: 10.1126/science.1169984 CrossRef Google Scholar
[36]	House C H, Beal E J, Orphan V J. The apparent involvement of ANMEs in mineral dependent methane oxidation, as an analog for possible martian methanotrophy [J]. Life, 2011, 1(1): 19-33. doi: 10.3390/life1010019 CrossRef Google Scholar
[37]	Oni O, Miyatake T, Kasten S, et al. Distinct microbial populations are tightly linked to the profile of dissolved iron in the methanic sediments of the Helgoland mud area, North Sea [J]. Frontiers in Microbiology, 2015, 6: 365. Google Scholar
[38]	Aromokeye D A, Kulkarni A C, Elvert M, et al. Rates and microbial players of iron-driven anaerobic oxidation of methane in methanic marine sediments [J]. Frontiers in Microbiology, 2020, 10: 3041. doi: 10.3389/fmicb.2019.03041 CrossRef Google Scholar
[39]	Scheller S, Yu H, Chadwick G L, et al. Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction [J]. Science, 2016, 351(6274): 703-707. doi: 10.1126/science.aad7154 CrossRef Google Scholar
[40]	Chang Y H, Cheng T W, Lai W J, et al. Microbial methane cycling in a terrestrial mud volcano in eastern Taiwan [J]. Environmental Microbiology, 2012, 14(4): 895-908. doi: 10.1111/j.1462-2920.2011.02658.x CrossRef Google Scholar
[41]	Kato S, Hirai M, Ohkuma M, et al. Microbial metabolisms in an abyssal ferromanganese crust from the Takuyo-Daigo seamount as revealed by metagenomics [J]. PLoS One, 2019, 14(11): e0224888. doi: 10.1371/journal.pone.0224888 CrossRef Google Scholar
[42]	Lipp J S, Morono Y, Inagaki F, et al. Significant contribution of Archaea to extant biomass in marine subsurface sediments [J]. Nature, 2008, 454(7207): 991-994. doi: 10.1038/nature07174 CrossRef Google Scholar
[43]	D’Hondt S, Jørgensen B B, Miller D J, et al. Distributions of microbial activities in deep subseafloor sediments [J]. Science, 2004, 306(5705): 2216-2221. doi: 10.1126/science.1101155 CrossRef Google Scholar
[44]	Vargas M, Kashefi K, Blunt-Harris E, et al. Microbiological evidence for Fe (III) reduction on early Earth [J]. Nature, 1998, 395(6697): 65-67. doi: 10.1038/25720 CrossRef Google Scholar
[45]	Peng X T, Guo Z X, Chen S, et al. Formation of carbonate pipes in the northern Okinawa Trough linked to strong sulfate exhaustion and iron supply [J]. Geochimica et Cosmochimica Acta, 2017, 205: 1-13. doi: 10.1016/j.gca.2017.02.010 CrossRef Google Scholar
[46]	Sun Z L, Wei H L, Zhang X H, et al. A unique Fe-rich carbonate chimney associated with cold seeps in the Northern Okinawa Trough, East China Sea [J]. Deep Sea Research Part I: Oceanographic Research Papers, 2015, 95: 37-53. doi: 10.1016/j.dsr.2014.10.005 CrossRef Google Scholar
[47]	Xie R, Wu D D, Liu J, et al. Geochemical evidence of metal-driven anaerobic oxidation of methane in the Shenhu area, the South China Sea [J]. International Journal of Environmental Research and Public Health, 2019, 16(19): 3559. doi: 10.3390/ijerph16193559 CrossRef Google Scholar
[48]	Liang L W, Wang Y Z, Sivan O, et al. Metal-dependent anaerobic methane oxidation in marine sediment: insights from marine settings and other systems [J]. Science China Life Sciences, 2019, 62(10): 1287-1295. doi: 10.1007/s11427-018-9554-5 CrossRef Google Scholar
[49]	Canfield D E. Reactive iron in marine sediments [J]. Geochimica et Cosmochimica Acta, 1989, 53(3): 619-632. doi: 10.1016/0016-7037(89)90005-7 CrossRef Google Scholar
[50]	Canfield D E, Raiswell R, Bottrell S H. The reactivity of sedimentary iron minerals toward sulfide [J]. American Journal of Science, 1992, 292(9): 659-683. doi: 10.2475/ajs.292.9.659 CrossRef Google Scholar
[51]	Vigderovich H, Liang L W, Herut B, et al. Evidence for microbial iron reduction in the methanogenic sediments of the oligotrophic SE Mediterranean continental shelf [J]. Biogeosciences Discuss, 2019, 16: 1-25. doi: 10.5194/bg-16-1-2019 CrossRef Google Scholar
[52]	Leu A O, Cai C, McIlroy S J, et al. Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae [J]. The ISME Journal, 2020, 14(4): 1030-1041. doi: 10.1038/s41396-020-0590-x CrossRef Google Scholar
[53]	Amos R T, Bekins B A, Cozzarelli I M, et al. Evidence for iron-mediated anaerobic methane oxidation in a crude oil-contaminated aquifer [J]. Geobiology, 2012, 10(6): 506-517. doi: 10.1111/j.1472-4669.2012.00341.x CrossRef Google Scholar
[54]	Fu L, Li S W, Ding Z W, et al. Iron reduction in the DAMO/Shewanella oneidensis MR-1 coculture system and the fate of Fe (II) [J]. Water Research, 2016, 88: 808-815. doi: 10.1016/j.watres.2015.11.011 CrossRef Google Scholar
[55]	McGlynn S E, Chadwick G L, Kempes C P, et al. Single cell activity reveals direct electron transfer in methanotrophic consortia [J]. Nature, 2015, 526(7574): 531-535. doi: 10.1038/nature15512 CrossRef Google Scholar
[56]	Kletzin A, Heimerl T, Flechsler J, et al. Cytochromes c in archaea: distribution, maturation, cell architecture, and the special case of Ignicoccus hospitalis [J]. Frontiers in Microbiology, 2015, 6: 439. Google Scholar
[57]	Roland F A E, Borges A V, Darchambeau F, et al. The possible occurrence of iron-dependent anaerobic methane oxidation in an Archean Ocean analogue [J]. Scientific Reports, 2021, 11(1): 1597. doi: 10.1038/s41598-021-81210-x CrossRef Google Scholar
[58]	Sivan O, Antler G, Turchyn A V, et al. Iron oxides stimulate sulfate-driven anaerobic methane oxidation in seeps [J]. Proceedings of the National Academy of Sciences of the United States of America, 2014, 111(40): E4139-E4147. doi: 10.1073/pnas.1412269111 CrossRef Google Scholar
[59]	Egger M, Hagens M, Sapart C J, et al. Iron oxide reduction in methane-rich deep Baltic Sea sediments [J]. Geochimica et Cosmochimica Acta, 2017, 207: 256-276. doi: 10.1016/j.gca.2017.03.019 CrossRef Google Scholar
[60]	Egger M, Rasigraf O, Sapart C J, et al. Iron-mediated anaerobic oxidation of methane in brackish coastal sediments [J]. Environmental Science & Technology, 2015, 49(1): 277-283. Google Scholar
[61]	Luo M, Torres M E, Hong W L, et al. Impact of iron release by volcanic ash alteration on carbon cycling in sediments of the northern Hikurangi margin [J]. Earth and Planetary Science Letters, 2020, 541: 116288. doi: 10.1016/j.jpgl.2020.116288 CrossRef Google Scholar
[62]	Tagliabue A, Bopp L, Dutay J C, et al. Hydrothermal contribution to the oceanic dissolved iron inventory [J]. Nature Geoscience, 2010, 3(4): 252-256. doi: 10.1038/ngeo818 CrossRef Google Scholar
[63]	McCollom T M, Shock E L. Geochemical constraints on chemolithoautotrophic metabolism by microorganisms in seafloor hydrothermal systems [J]. Geochimica et Cosmochimica Acta, 1997, 61(20): 4375-4391. doi: 10.1016/S0016-7037(97)00241-X CrossRef Google Scholar
[64]	Sun Z L, Wu N Y, Cao H, et al. Hydrothermal metal supplies enhance the benthic methane filter in oceans: An example from the Okinawa Trough [J]. Chemical Geology, 2019, 525: 190-209. doi: 10.1016/j.chemgeo.2019.07.025 CrossRef Google Scholar
[65]	吴能友, 孙治雷, 卢建国, 等. 冲绳海槽海底冷泉-热液系统相互作用[J]. 海洋地质与第四纪地质, 2019, 39(5):23-35 Google Scholar WU Nengyou, SUN Zhilei, LU Jianguo, et al. Interaction between seafloor cold seeps and adjacent hydrothermal activities in the Okinawa Trough [J]. Marine Geology & Quaternary Geology, 2019, 39(5): 23-35. Google Scholar
[66]	McCollom T M. Geochemical constraints on primary productivity in submarine hydrothermal vent plumes [J]. Deep Sea Research Part I: Oceanographic Research Papers, 2000, 47(1): 85-101. doi: 10.1016/S0967-0637(99)00048-5 CrossRef Google Scholar
[67]	Ruff S E, Bidle J F, Teske A P, et al. Global dispersion and local diversification of the methane seep microbiome [J]. Proceedings of the National Academy of Sciences of the United States of America, 2015, 112(13): 4015-4020. doi: 10.1073/pnas.1421865112 CrossRef Google Scholar
[68]	Hubert C, Loy A, Nickel M, et al. A constant flux of diverse thermophilic bacteria into the cold Arctic seabed [J]. Science, 2009, 325(5947): 1541-1544. doi: 10.1126/science.1174012 CrossRef Google Scholar
[69]	Schauer R, Bienhold C, Ramette A, et al. Bacterial diversity and biogeography in deep-sea surface sediments of the South Atlantic Ocean [J]. The ISME Journal, 2010, 4(2): 159-170. doi: 10.1038/ismej.2009.106 CrossRef Google Scholar