New Insights into the Ecology and Physiology of Methanomassiliicoccales from Terrestrial and Aquatic Environments

Type Article
Date 2021-01
Language English
Author(s) Cozannet MarcORCID3, Borrel Guillaume2, Roussel Erwan1, Moalic YannORCID3, Allioux Maxime3, Sanvoisin Amandine2, Toffin Laurent1, Alain Karine4
Affiliation(s) 1 : Laboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, France
2 : Unit Evolutionary Biology of the Microbial Cell, Department of Microbiology, Institute Pasteur, 75015 Paris, France
3 : Laboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, France
4 : Laboratoire de Microbiologie des Environnements Extrêmes LM2E, Univ Brest, CNRS, IFREMER, IRP 1211 MicrobSea, UMR 6197, IUEM, Rue Dumont d’Urville, F-29280 Plouzané, France
Source Microorganisms (2076-2607) (MDPI), 2021-01 , Vol. 9 , N. 1 , P. 30 (31p.)
DOI 10.3390/microorganisms9010030
Note This article belongs to the Section Environmental Microbiology
Keyword(s) Methanomassiliicoccales, cultivation, methyl-compounds, environmental cluster, networks
Abstract

Members of the archaeal order Methanomassiliicoccales 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 Methanomassiliicoccales were very scarce in most terrestrial and aquatic ecosystems. Relative abundance of Methanomassiliicoccales and substrates/products of methanogenesis were monitored during incubation of environmental slurries. A sediment slurry enriched in Methanomassiliicoccales 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 Candidatus ‘Methanomassiliicoccus armoricus MXMAG1’. Comparison of the annotated genome of MXMAG1 with the published genomes and MAGs from Methanomassiliicoccales 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 Candidatus ‘M. armoricus MXMAG1’. As expected, Ca. ‘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 Methanomassiliicoccales 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.

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