Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps
Methane seeps are widespread seafloor ecosystems shaped by complex physicochemical-biological interactions over geological timescales, and seep microbiomes play a vital role in global biogeochemical cycling of key elements on Earth. However, the mechanisms underlying the coexistence of methane-cycli...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2020-07-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmicb.2020.01409/full |
| _version_ | 1818292754463064064 |
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| author | Haizhou Li Qunhui Yang Huaiyang Zhou |
| author_facet | Haizhou Li Qunhui Yang Huaiyang Zhou |
| author_sort | Haizhou Li |
| collection | DOAJ |
| description | Methane seeps are widespread seafloor ecosystems shaped by complex physicochemical-biological interactions over geological timescales, and seep microbiomes play a vital role in global biogeochemical cycling of key elements on Earth. However, the mechanisms underlying the coexistence of methane-cycling microbial communities remain largely elusive. Here, high-resolution sediment incubation experiments revealed a cryptic methane cycle in the South China Sea (SCS) methane seep ecosystem, showing the coexistence of sulfate (SO42–)- or iron (Fe)-dependent anaerobic oxidation of methane (AOM) and methylotrophic methanogenesis. This previously unrecognized methane cycling is not discernible from geochemical profiles due to high net methane consumption. High-throughput sequencing and Catalyzed Reporter Deposition-Fluorescence in situ Hybridization (CARD-FISH) results suggested that anaerobic methane-oxidizing archaea (ANME)-2 and -3 coupled to sulfate-reducing bacteria (SRB) carried out SO42–-AOM, and alternative ANME-2 and -3 solely or coupled to iron-reducing bacteria (IRB) might participate in Fe-AOM in sulfate-depleted environments. This finding suggested that ANME could alter AOM metabolic pathways according to geochemical changes. Furthermore, the majority of methylotrophic methanogens belonged to Methanimicrococcus, and hydrogenotrophic and acetoclastic methanogens were likely inhibited by sulfate or iron respiration. Fe-AOM and methylotrophic methanogenesis are overlooked potential sources and sinks of methane in methane seep ecosystems, thus influencing methane budgets and even the global carbon budget in the ocean. |
| first_indexed | 2024-12-13T03:04:59Z |
| format | Article |
| id | doaj.art-fc84a4bbbd5d44b5a5c945920a68710d |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-13T03:04:59Z |
| publishDate | 2020-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-fc84a4bbbd5d44b5a5c945920a68710d2022-12-22T00:01:45ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2020-07-011110.3389/fmicb.2020.01409524011Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane SeepsHaizhou LiQunhui YangHuaiyang ZhouMethane seeps are widespread seafloor ecosystems shaped by complex physicochemical-biological interactions over geological timescales, and seep microbiomes play a vital role in global biogeochemical cycling of key elements on Earth. However, the mechanisms underlying the coexistence of methane-cycling microbial communities remain largely elusive. Here, high-resolution sediment incubation experiments revealed a cryptic methane cycle in the South China Sea (SCS) methane seep ecosystem, showing the coexistence of sulfate (SO42–)- or iron (Fe)-dependent anaerobic oxidation of methane (AOM) and methylotrophic methanogenesis. This previously unrecognized methane cycling is not discernible from geochemical profiles due to high net methane consumption. High-throughput sequencing and Catalyzed Reporter Deposition-Fluorescence in situ Hybridization (CARD-FISH) results suggested that anaerobic methane-oxidizing archaea (ANME)-2 and -3 coupled to sulfate-reducing bacteria (SRB) carried out SO42–-AOM, and alternative ANME-2 and -3 solely or coupled to iron-reducing bacteria (IRB) might participate in Fe-AOM in sulfate-depleted environments. This finding suggested that ANME could alter AOM metabolic pathways according to geochemical changes. Furthermore, the majority of methylotrophic methanogens belonged to Methanimicrococcus, and hydrogenotrophic and acetoclastic methanogens were likely inhibited by sulfate or iron respiration. Fe-AOM and methylotrophic methanogenesis are overlooked potential sources and sinks of methane in methane seep ecosystems, thus influencing methane budgets and even the global carbon budget in the ocean.https://www.frontiersin.org/article/10.3389/fmicb.2020.01409/fullmethane seepsSouth China Seaanaerobic oxidation of methanemethylotrophic methanogenesissulfate reductioniron reduction |
| spellingShingle | Haizhou Li Qunhui Yang Huaiyang Zhou Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps Frontiers in Microbiology methane seeps South China Sea anaerobic oxidation of methane methylotrophic methanogenesis sulfate reduction iron reduction |
| title | Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps |
| title_full | Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps |
| title_fullStr | Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps |
| title_full_unstemmed | Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps |
| title_short | Niche Differentiation of Sulfate- and Iron-Dependent Anaerobic Methane Oxidation and Methylotrophic Methanogenesis in Deep Sea Methane Seeps |
| title_sort | niche differentiation of sulfate and iron dependent anaerobic methane oxidation and methylotrophic methanogenesis in deep sea methane seeps |
| topic | methane seeps South China Sea anaerobic oxidation of methane methylotrophic methanogenesis sulfate reduction iron reduction |
| url | https://www.frontiersin.org/article/10.3389/fmicb.2020.01409/full |
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