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

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.

SUBMITTER: Cozannet M

PROVIDER: S-EPMC7824343 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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

Cozannet Marc M Borrel Guillaume G Roussel Erwan E Moalic Yann Y Allioux Maxime M Sanvoisin Amandine A Toffin Laurent L Alain Karine K

Microorganisms 20201224 1

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 aqua ...[more]

PMID: 33374130

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Project description:The globally distributed green microalga Chlorella vulgaris (Chlorophyta) colonizes aquatic and terrestrial habitats, but the molecular mechanisms underpinning survival in these two contrasting environments are far from understood. Here, we compared the authentic strain of C. vulgaris from an aquatic habitat with a strain from a terrestrial high alpine habitat previously determined as Chlorella mirabilis. Molecular phylogeny of SSU rDNA (823 bp) showed that the two strains differed by one nucleotide only. Sequencing of the ITS2 region confirmed that both strains belong to the same species, but to distinct ribotypes. Therefore, the terrestrial strain was re-assessed as C. vulgaris. To study the response to environmental conditions experienced on land, we assessed the effects of irradiance and temperature on growth, of temperature on photosynthesis and respiration, and of desiccation and rehydration on photosynthetic performance. In contrast to the aquatic strain, the terrestrial strain tolerated higher temperatures and light conditions, had a higher photosynthesis-to-respiration ratio at 25°C, still grew at 30°C and was able to fully recover photosynthetic performance after desiccation at 84% relative humidity. The two strains differed most in their response to the dehydration/rehydration treatment, which was further investigated by untargeted GC-MS-based metabolite profiling to gain insights into metabolic traits differentiating the two strains. The two strains differed in their allocation of carbon and nitrogen into their primary metabolites. Overall, the terrestrial strain had higher contents of readily available nitrogen-based metabolites, especially amino acids and the polyamine putrescine. Dehydration and rehydration led to differential regulation of the amino acid metabolism, the tricarboxylic acid cycle and sucrose metabolism. The data are discussed with a view to differences in phenotypic plasticity of the two strains, and we suggest that the two genetically almost identical C. vulgaris strains are attractive models to study mechanisms that protect from abiotic stress factors, which are more frequent in terrestrial than aquatic habitats, such as desiccation and irradiation.

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

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New Insights into the Ecology and Physiology of <i>Methanomassiliicoccales</i> from Terrestrial and Aquatic Environments.

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