Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>
ABSTRACT Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and mang...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2020-06-01
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| Series: | mBio |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/mBio.01325-20 |
| _version_ | 1818740146666733568 |
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| author | Andy O. Leu Simon J. McIlroy Jun Ye Donovan H. Parks Victoria J. Orphan Gene W. Tyson |
| author_facet | Andy O. Leu Simon J. McIlroy Jun Ye Donovan H. Parks Victoria J. Orphan Gene W. Tyson |
| author_sort | Andy O. Leu |
| collection | DOAJ |
| description | ABSTRACT Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceae metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate and the reduction of arsenate, selenate, and elemental sulfur. Numerous membrane-bound multiheme c-type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humic substances, and syntrophic partners. IMPORTANCE AOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance for the global carbon cycle and climate change modeling. While the oxidation of methane coupled to sulfate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study, we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae, as they are absent from related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles. |
| first_indexed | 2024-12-18T01:36:06Z |
| format | Article |
| id | doaj.art-26da6f3997eb47a88cc7c200bb1d380d |
| institution | Directory Open Access Journal |
| issn | 2150-7511 |
| language | English |
| last_indexed | 2024-12-18T01:36:06Z |
| publishDate | 2020-06-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mBio |
| spelling | doaj.art-26da6f3997eb47a88cc7c200bb1d380d2022-12-21T21:25:26ZengAmerican Society for MicrobiologymBio2150-75112020-06-0111310.1128/mBio.01325-20Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic>Andy O. Leu0Simon J. McIlroy1Jun Ye2Donovan H. Parks3Victoria J. Orphan4Gene W. Tyson5Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, AustraliaAustralian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, AustraliaAustralian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, AustraliaAustralian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, AustraliaDepartment of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USAAustralian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, St. Lucia, AustraliaABSTRACT Anaerobic oxidation of methane (AOM) is an important biological process responsible for controlling the flux of methane into the atmosphere. Members of the archaeal family Methanoperedenaceae (formerly ANME-2d) have been demonstrated to couple AOM to the reduction of nitrate, iron, and manganese. Here, comparative genomic analysis of 16 Methanoperedenaceae metagenome-assembled genomes (MAGs), recovered from diverse environments, revealed novel respiratory strategies acquired through lateral gene transfer (LGT) events from diverse archaea and bacteria. Comprehensive phylogenetic analyses suggests that LGT has allowed members of the Methanoperedenaceae to acquire genes for the oxidation of hydrogen and formate and the reduction of arsenate, selenate, and elemental sulfur. Numerous membrane-bound multiheme c-type cytochrome complexes also appear to have been laterally acquired, which may be involved in the direct transfer of electrons to metal oxides, humic substances, and syntrophic partners. IMPORTANCE AOM by microorganisms limits the atmospheric release of the potent greenhouse gas methane and has consequent importance for the global carbon cycle and climate change modeling. While the oxidation of methane coupled to sulfate by consortia of anaerobic methanotrophic (ANME) archaea and bacteria is well documented, several other potential electron acceptors have also been reported to support AOM. In this study, we identify a number of novel respiratory strategies that appear to have been laterally acquired by members of the Methanoperedenaceae, as they are absent from related archaea and other ANME lineages. Expanding the known metabolic potential for members of the Methanoperedenaceae provides important insight into their ecology and suggests their role in linking methane oxidation to several global biogeochemical cycles.https://journals.asm.org/doi/10.1128/mBio.01325-20ANMEAOMcomparative genomicsmethaneMethanoperedenaceae |
| spellingShingle | Andy O. Leu Simon J. McIlroy Jun Ye Donovan H. Parks Victoria J. Orphan Gene W. Tyson Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic> mBio ANME AOM comparative genomics methane Methanoperedenaceae |
| title | Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic> |
| title_full | Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic> |
| title_fullStr | Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic> |
| title_full_unstemmed | Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic> |
| title_short | Lateral Gene Transfer Drives Metabolic Flexibility in the Anaerobic Methane-Oxidizing Archaeal Family <italic toggle="yes">Methanoperedenaceae</italic> |
| title_sort | lateral gene transfer drives metabolic flexibility in the anaerobic methane oxidizing archaeal family italic toggle yes methanoperedenaceae italic |
| topic | ANME AOM comparative genomics methane Methanoperedenaceae |
| url | https://journals.asm.org/doi/10.1128/mBio.01325-20 |
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