Information on the biochemical pathways of carbon and energy metabolism in representatives of the deep lineage bacterial phylum Deferribacteres are scarce. Here, we report the results of the sequencing and analysis of the high-quality draft genome of the thermophilic chemolithoautotrophic anaerobe Deferribacter autotrophicus. Genomic data suggest that CO2 assimilation is carried out by recently proposed reversible tricarboxylic acid cycle (“roTCA cycle”). The predicted genomic ability of D. autotrophicus to grow due to the oxidation of carbon monoxide was experimentally proven. CO oxidation was coupled with the reduction of nitrate to ammonium. Utilization of CO most likely involves anaerobic [Ni, Fe]-containing CO dehydrogenase. This is the first evidence of CO oxidation in the phylum Deferribacteres. The genome of D. autotrophicus encodes a Nap-type complex of nitrate reduction. However, the conversion of produced nitrite to ammonium proceeds via a non-canonical pathway with the participation of hydroxylamine oxidoreductase (Hao) and hydroxylamine reductase. The genome contains 17 genes of putative multiheme c-type cytochromes and “e-pilin” genes, some of which are probably involved in Fe(III) reduction. Genomic analysis indicates that the roTCA cycle of CO2 fixation and putative Hao-enabled ammonification may occur in several members of the phylum Deferribacteres.

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.

Marine hydrothermal systems are characterized by a pronounced biogeochemical sulfur cycle with the participation of sulfur-oxidizing, sulfate-reducing and sulfur-disproportionating microorganisms. The diversity and metabolism of sulfur disproportionators are studied to a much lesser extent compared with other microbial groups. Dissulfurirhabdus thermomarina SH388T is an anaerobic thermophilic bacterium isolated from a shallow sea hydrothermal vent. D. thermomarina is an obligate chemolithoautotroph able to grow by the disproportionation of sulfite and elemental sulfur. Here, we present the results of the sequencing and analysis of the high-quality draft genome of strain SH388T. The genome consists of a one circular chromosome of 2,461,642 base pairs, has a G + C content of 71.1 mol% and 2267 protein-coding sequences. The genome analysis revealed a complete set of genes essential to CO2 fixation via the reductive acetyl-CoA (Wood-Ljungdahl) pathway and gluconeogenesis. The genome of D. thermomarina encodes a complete set of genes necessary for the dissimilatory reduction of sulfates, which are probably involved in the disproportionation of sulfur. Data on the occurrences of Dissulfurirhabdus 16S rRNA gene sequences in gene libraries and metagenome datasets showed the worldwide distribution of the members of this genus. This study expands our knowledge of the microbial contribution into carbon and sulfur cycles in the marine hydrothermal environments.