New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments
Members of the archaeal order <i>Methanomassiliicoccales</i> are methanogens mainly associated with animal digestive tracts. However, environmental members remain poorly characterized as no representatives not associated with a host have been cultivated so far. In this study, metabarcodi...
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MDPI AG
2020-12-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/9/1/30 |
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| author | Marc Cozannet Guillaume Borrel Erwan Roussel Yann Moalic Maxime Allioux Amandine Sanvoisin Laurent Toffin Karine Alain |
| author_facet | Marc Cozannet Guillaume Borrel Erwan Roussel Yann Moalic Maxime Allioux Amandine Sanvoisin Laurent Toffin Karine Alain |
| author_sort | Marc Cozannet |
| collection | DOAJ |
| description | Members of the archaeal order <i>Methanomassiliicoccales</i> are methanogens mainly associated with animal digestive tracts. However, environmental members remain poorly characterized as no representatives not associated with a host have been cultivated so far. In this study, metabarcoding screening combined with quantitative PCR analyses on a collection of diverse non-host-associated environmental samples revealed that <i>Methanomassiliicoccales</i> were very scarce in most terrestrial and aquatic ecosystems. Relative abundance of <i>Methanomassiliicoccales</i> and substrates/products of methanogenesis were monitored during incubation of environmental slurries. A sediment slurry enriched in <i>Methanomassiliicoccales</i> was obtained from a freshwater sample. It allowed the reconstruction of a high-quality metagenome-assembled genome (MAG) corresponding to a new candidate species, for which we propose the name of <i>Candidatus</i> ‘Methanomassiliicoccus armoricus MXMAG1’. Comparison of the annotated genome of MXMAG1 with the published genomes and MAGs from <i>Methanomassiliicoccales</i> belonging to the 2 known clades (‘free-living’/non-host-associated environmental clade and ‘host-associated’/digestive clade) allowed us to explore the putative physiological traits of <i>Candidatus</i> ‘M. armoricus MXMAG1’. As expected, <i>Ca.</i> ‘Methanomassiliicoccus armoricus MXMAG1’ had the genetic potential to produce methane by reduction of methyl compounds and dihydrogen oxidation. This MAG encodes for several putative physiological and stress response adaptations, including biosynthesis of trehalose (osmotic and temperature regulations), agmatine production (pH regulation), and arsenic detoxication, by reduction and excretion of arsenite, a mechanism that was only present in the ‘free-living’ clade. An analysis of co-occurrence networks carried out on environmental samples and slurries also showed that <i>Methanomassiliicoccales</i> detected in terrestrial and aquatic ecosystems were strongly associated with acetate and dihydrogen producing bacteria commonly found in digestive habitats and which have been reported to form syntrophic relationships with methanogens. |
| first_indexed | 2024-03-10T13:48:41Z |
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| id | doaj.art-bdc081d3e57d44f4b454366a50411e81 |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-10T13:48:41Z |
| publishDate | 2020-12-01 |
| publisher | MDPI AG |
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| series | Microorganisms |
| spelling | doaj.art-bdc081d3e57d44f4b454366a50411e812023-11-21T02:21:09ZengMDPI AGMicroorganisms2076-26072020-12-01913010.3390/microorganisms9010030New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic EnvironmentsMarc Cozannet0Guillaume Borrel1Erwan Roussel2Yann Moalic3Maxime Allioux4Amandine Sanvoisin5Laurent Toffin6Karine Alain7Laboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, FranceUnit Evolutionary Biology of the Microbial Cell, Department of Microbiology, Institute Pasteur, 75015 Paris, FranceLaboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, FranceLaboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, FranceLaboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, FranceLaboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, FranceLaboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, FranceLaboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, FranceMembers of the archaeal order <i>Methanomassiliicoccales</i> are methanogens mainly associated with animal digestive tracts. However, environmental members remain poorly characterized as no representatives not associated with a host have been cultivated so far. In this study, metabarcoding screening combined with quantitative PCR analyses on a collection of diverse non-host-associated environmental samples revealed that <i>Methanomassiliicoccales</i> were very scarce in most terrestrial and aquatic ecosystems. Relative abundance of <i>Methanomassiliicoccales</i> and substrates/products of methanogenesis were monitored during incubation of environmental slurries. A sediment slurry enriched in <i>Methanomassiliicoccales</i> was obtained from a freshwater sample. It allowed the reconstruction of a high-quality metagenome-assembled genome (MAG) corresponding to a new candidate species, for which we propose the name of <i>Candidatus</i> ‘Methanomassiliicoccus armoricus MXMAG1’. Comparison of the annotated genome of MXMAG1 with the published genomes and MAGs from <i>Methanomassiliicoccales</i> belonging to the 2 known clades (‘free-living’/non-host-associated environmental clade and ‘host-associated’/digestive clade) allowed us to explore the putative physiological traits of <i>Candidatus</i> ‘M. armoricus MXMAG1’. As expected, <i>Ca.</i> ‘Methanomassiliicoccus armoricus MXMAG1’ had the genetic potential to produce methane by reduction of methyl compounds and dihydrogen oxidation. This MAG encodes for several putative physiological and stress response adaptations, including biosynthesis of trehalose (osmotic and temperature regulations), agmatine production (pH regulation), and arsenic detoxication, by reduction and excretion of arsenite, a mechanism that was only present in the ‘free-living’ clade. An analysis of co-occurrence networks carried out on environmental samples and slurries also showed that <i>Methanomassiliicoccales</i> detected in terrestrial and aquatic ecosystems were strongly associated with acetate and dihydrogen producing bacteria commonly found in digestive habitats and which have been reported to form syntrophic relationships with methanogens.https://www.mdpi.com/2076-2607/9/1/30<i>Methanomassiliicoccales</i>cultivationmethyl-compoundsenvironmental clusternetworks |
| spellingShingle | Marc Cozannet Guillaume Borrel Erwan Roussel Yann Moalic Maxime Allioux Amandine Sanvoisin Laurent Toffin Karine Alain New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments Microorganisms <i>Methanomassiliicoccales</i> cultivation methyl-compounds environmental cluster networks |
| title | New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments |
| title_full | New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments |
| title_fullStr | New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments |
| title_full_unstemmed | New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments |
| title_short | New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments |
| title_sort | new insights into the ecology and physiology of i methanomassiliicoccales i from terrestrial and aquatic environments |
| topic | <i>Methanomassiliicoccales</i> cultivation methyl-compounds environmental cluster networks |
| url | https://www.mdpi.com/2076-2607/9/1/30 |
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