Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria
The key microbial group involved in anaerobic methane oxidation is anaerobic methanotrophic archaea (ANME). From a terrestrial mud volcano, we enriched a microbial community containing ANME-2a, using methane as an electron donor, Fe(III) oxide (ferrihydrite) as an electron acceptor, and anthraquinon...
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MDPI AG
2023-02-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/11/3/555 |
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| author | Alexander I. Slobodkin Nataliya M. Ratnikova Galina B. Slobodkina Alexandra A. Klyukina Nikolay A. Chernyh Alexander Y. Merkel |
| author_facet | Alexander I. Slobodkin Nataliya M. Ratnikova Galina B. Slobodkina Alexandra A. Klyukina Nikolay A. Chernyh Alexander Y. Merkel |
| author_sort | Alexander I. Slobodkin |
| collection | DOAJ |
| description | The key microbial group involved in anaerobic methane oxidation is anaerobic methanotrophic archaea (ANME). From a terrestrial mud volcano, we enriched a microbial community containing ANME-2a, using methane as an electron donor, Fe(III) oxide (ferrihydrite) as an electron acceptor, and anthraquinone-2,6-disulfonate as an electron shuttle. Ferrihydrite reduction led to the formation of a black, highly magnetic precipitate. A significant relative abundance of ANME-2a in batch cultures was observed over five subsequent transfers. Phylogenetic analysis revealed that, in addition to ANME-2a, two bacterial taxa belonging to uncultured <i>Desulfobulbaceae</i> and <i>Anaerolineaceae</i> were constantly present in all enrichments. Metagenome-assembled genomes (MAGs) of ANME-2a contained a complete set of genes for methanogenesis and numerous genes of multiheme c-type cytochromes (MHC), indicating the capability of methanotrophs to transfer electrons to metal oxides or to a bacterial partner. One of the ANME MAGs encoded respiratory arsenate reductase (Arr), suggesting the potential for a direct coupling of methane oxidation with As(V) reduction in the single microorganism. The same MAG also encoded uptake [NiFe] hydrogenase, which is uncommon for ANME-2. The MAG of uncultured <i>Desulfobulbaceae</i> contained genes of dissimilatory sulfate reduction, a Wood–Ljungdahl pathway for autotrophic CO<sub>2</sub> fixation, hydrogenases, and 43 MHC. We hypothesize that uncultured <i>Desulfobulbaceae</i> is a bacterial partner of ANME-2a, which mediates extracellular electron transfer to Fe(III) oxide. |
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| format | Article |
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| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-11T06:09:07Z |
| publishDate | 2023-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-3caa6967a123468f85fa79aa9feba1082023-11-17T12:44:47ZengMDPI AGMicroorganisms2076-26072023-02-0111355510.3390/microorganisms11030555Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated BacteriaAlexander I. Slobodkin0Nataliya M. Ratnikova1Galina B. Slobodkina2Alexandra A. Klyukina3Nikolay A. Chernyh4Alexander Y. Merkel5Winogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaWinogradsky Institute of Microbiology, Research Center of Biotechnology, Russian Academy of Sciences, Leninskiy Prospect, 33, Bld. 2, 119071 Moscow, RussiaThe key microbial group involved in anaerobic methane oxidation is anaerobic methanotrophic archaea (ANME). From a terrestrial mud volcano, we enriched a microbial community containing ANME-2a, using methane as an electron donor, Fe(III) oxide (ferrihydrite) as an electron acceptor, and anthraquinone-2,6-disulfonate as an electron shuttle. Ferrihydrite reduction led to the formation of a black, highly magnetic precipitate. A significant relative abundance of ANME-2a in batch cultures was observed over five subsequent transfers. Phylogenetic analysis revealed that, in addition to ANME-2a, two bacterial taxa belonging to uncultured <i>Desulfobulbaceae</i> and <i>Anaerolineaceae</i> were constantly present in all enrichments. Metagenome-assembled genomes (MAGs) of ANME-2a contained a complete set of genes for methanogenesis and numerous genes of multiheme c-type cytochromes (MHC), indicating the capability of methanotrophs to transfer electrons to metal oxides or to a bacterial partner. One of the ANME MAGs encoded respiratory arsenate reductase (Arr), suggesting the potential for a direct coupling of methane oxidation with As(V) reduction in the single microorganism. The same MAG also encoded uptake [NiFe] hydrogenase, which is uncommon for ANME-2. The MAG of uncultured <i>Desulfobulbaceae</i> contained genes of dissimilatory sulfate reduction, a Wood–Ljungdahl pathway for autotrophic CO<sub>2</sub> fixation, hydrogenases, and 43 MHC. We hypothesize that uncultured <i>Desulfobulbaceae</i> is a bacterial partner of ANME-2a, which mediates extracellular electron transfer to Fe(III) oxide.https://www.mdpi.com/2076-2607/11/3/555methaneAOMmud volcanomicrobial communitiesANMEarchaea |
| spellingShingle | Alexander I. Slobodkin Nataliya M. Ratnikova Galina B. Slobodkina Alexandra A. Klyukina Nikolay A. Chernyh Alexander Y. Merkel Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria Microorganisms methane AOM mud volcano microbial communities ANME archaea |
| title | Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria |
| title_full | Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria |
| title_fullStr | Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria |
| title_full_unstemmed | Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria |
| title_short | Composition and Metabolic Potential of Fe(III)-Reducing Enrichment Cultures of Methanotrophic ANME-2a Archaea and Associated Bacteria |
| title_sort | composition and metabolic potential of fe iii reducing enrichment cultures of methanotrophic anme 2a archaea and associated bacteria |
| topic | methane AOM mud volcano microbial communities ANME archaea |
| url | https://www.mdpi.com/2076-2607/11/3/555 |
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