Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane
In seafloor sediments, the anaerobic oxidation of methane (AOM) consumes most of the methane formed in anoxic layers, preventing this greenhouse gas from reaching the water column and finally the atmosphere. AOM is performed by syntrophic consortia of specific anaerobic methane-oxidizing archaea (AN...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2022.988871/full |
| _version_ | 1818058237466902528 |
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| author | David Benito Merino David Benito Merino Hanna Zehnle Hanna Zehnle Hanna Zehnle Andreas Teske Gunter Wegener Gunter Wegener |
| author_facet | David Benito Merino David Benito Merino Hanna Zehnle Hanna Zehnle Hanna Zehnle Andreas Teske Gunter Wegener Gunter Wegener |
| author_sort | David Benito Merino |
| collection | DOAJ |
| description | In seafloor sediments, the anaerobic oxidation of methane (AOM) consumes most of the methane formed in anoxic layers, preventing this greenhouse gas from reaching the water column and finally the atmosphere. AOM is performed by syntrophic consortia of specific anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). Cultures with diverse AOM partners exist at temperatures between 12°C and 60°C. Here, from hydrothermally heated sediments of the Guaymas Basin, we cultured deep-branching ANME-1c that grow in syntrophic consortia with Thermodesulfobacteria at 70°C. Like all ANME, ANME-1c oxidize methane using the methanogenesis pathway in reverse. As an uncommon feature, ANME-1c encode a nickel-iron hydrogenase. This hydrogenase has low expression during AOM and the partner Thermodesulfobacteria lack hydrogen-consuming hydrogenases. Therefore, it is unlikely that the partners exchange hydrogen during AOM. ANME-1c also does not consume hydrogen for methane formation, disputing a recent hypothesis on facultative methanogenesis. We hypothesize that the ANME-1c hydrogenase might have been present in the common ancestor of ANME-1 but lost its central metabolic function in ANME-1c archaea. For potential direct interspecies electron transfer (DIET), both partners encode and express genes coding for extracellular appendages and multiheme cytochromes. Thermodesulfobacteria encode and express an extracellular pentaheme cytochrome with high similarity to cytochromes of other syntrophic sulfate-reducing partner bacteria. ANME-1c might associate specifically to Thermodesulfobacteria, but their co-occurrence is so far only documented for heated sediments of the Gulf of California. However, in the deep seafloor, sulfate–methane interphases appear at temperatures up to 80°C, suggesting these as potential habitats for the partnership of ANME-1c and Thermodesulfobacteria. |
| first_indexed | 2024-12-10T12:57:26Z |
| format | Article |
| id | doaj.art-87598eb027cf4db2a909b4ca77f1b35c |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-12-10T12:57:26Z |
| publishDate | 2022-09-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Microbiology |
| spelling | doaj.art-87598eb027cf4db2a909b4ca77f1b35c2022-12-22T01:48:03ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2022-09-011310.3389/fmicb.2022.988871988871Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methaneDavid Benito Merino0David Benito Merino1Hanna Zehnle2Hanna Zehnle3Hanna Zehnle4Andreas Teske5Gunter Wegener6Gunter Wegener7Max Planck Institute for Marine Microbiology, Bremen, GermanyFaculty of Geosciences, University of Bremen, Bremen, GermanyMax Planck Institute for Marine Microbiology, Bremen, GermanyFaculty of Geosciences, University of Bremen, Bremen, GermanyMARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, GermanyDepartment of Earth, Marine and Environmental Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, United StatesMax Planck Institute for Marine Microbiology, Bremen, GermanyMARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, GermanyIn seafloor sediments, the anaerobic oxidation of methane (AOM) consumes most of the methane formed in anoxic layers, preventing this greenhouse gas from reaching the water column and finally the atmosphere. AOM is performed by syntrophic consortia of specific anaerobic methane-oxidizing archaea (ANME) and sulfate-reducing bacteria (SRB). Cultures with diverse AOM partners exist at temperatures between 12°C and 60°C. Here, from hydrothermally heated sediments of the Guaymas Basin, we cultured deep-branching ANME-1c that grow in syntrophic consortia with Thermodesulfobacteria at 70°C. Like all ANME, ANME-1c oxidize methane using the methanogenesis pathway in reverse. As an uncommon feature, ANME-1c encode a nickel-iron hydrogenase. This hydrogenase has low expression during AOM and the partner Thermodesulfobacteria lack hydrogen-consuming hydrogenases. Therefore, it is unlikely that the partners exchange hydrogen during AOM. ANME-1c also does not consume hydrogen for methane formation, disputing a recent hypothesis on facultative methanogenesis. We hypothesize that the ANME-1c hydrogenase might have been present in the common ancestor of ANME-1 but lost its central metabolic function in ANME-1c archaea. For potential direct interspecies electron transfer (DIET), both partners encode and express genes coding for extracellular appendages and multiheme cytochromes. Thermodesulfobacteria encode and express an extracellular pentaheme cytochrome with high similarity to cytochromes of other syntrophic sulfate-reducing partner bacteria. ANME-1c might associate specifically to Thermodesulfobacteria, but their co-occurrence is so far only documented for heated sediments of the Gulf of California. However, in the deep seafloor, sulfate–methane interphases appear at temperatures up to 80°C, suggesting these as potential habitats for the partnership of ANME-1c and Thermodesulfobacteria.https://www.frontiersin.org/articles/10.3389/fmicb.2022.988871/fullanaerobic oxidation of methaneANME-1archaeadeep seahydrothermal vents |
| spellingShingle | David Benito Merino David Benito Merino Hanna Zehnle Hanna Zehnle Hanna Zehnle Andreas Teske Gunter Wegener Gunter Wegener Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane Frontiers in Microbiology anaerobic oxidation of methane ANME-1 archaea deep sea hydrothermal vents |
| title | Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane |
| title_full | Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane |
| title_fullStr | Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane |
| title_full_unstemmed | Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane |
| title_short | Deep-branching ANME-1c archaea grow at the upper temperature limit of anaerobic oxidation of methane |
| title_sort | deep branching anme 1c archaea grow at the upper temperature limit of anaerobic oxidation of methane |
| topic | anaerobic oxidation of methane ANME-1 archaea deep sea hydrothermal vents |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2022.988871/full |
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