Gavrilov, Sergey N.

The anaerobic oxidation of fatty acids and alcohols occurs near the thermodynamic limit of life. This process is driven by syntrophic bacteria that oxidize fatty acids and/or alcohols, their syntrophic partners that consume the products of this oxidation, and the pathways for interspecies electron exchange via these products or direct interspecies electron transfer (DIET). Due to the interdependence of syntrophic microorganisms on each other’s metabolic activity, their isolation in pure cultures is almost impossible. Thus, little is known about their physiology, and the only available way to fill in the knowledge gap on these organisms is genomic and metabolic analysis of syntrophic cultures. Here we report the results of genome sequencing and analysis of an obligately syntrophic alkaliphilic bacterium ‘Candidatus Contubernalis alkaliaceticus’. The genomic data suggest that acetate oxidation is carried out by the Wood–Ljungdahl pathway, while a bimodular respiratory system involving an Rnf complex and a Na+-dependent ATP synthase is used for energy conservation. The predicted genomic ability of ‘Ca. C. alkaliaceticus’ to outperform interspecies electron transfer both indirectly, via H2 or formate, and directly, via pili-like appendages of its syntrophic partner or conductive mineral particles, was experimentally demonstrated. This is the first indication of DIET in the class Dethiobacteria.

SummaryA novel moderately thermophilic, facultatively anaerobic chemoorganotrophic bacterium strainP3M‐2Twas isolated from a microbial mat developing on the wooden surface of a chute under the flow of hot water (46°C) coming out of a 2775‐m‐deep oil exploration well (Tomsk region,Russia). StrainP3M‐2Tis a moderate thermophile and facultative anaerobe growing on mono‐, di‐ or polysaccharides by aerobic respiration, fermentation or by reducing diverse electron acceptors [nitrite,Fe(III),As(V)]. Its closest cultivated relative (90.8%rRNAgene sequence identity) isIgnavibacterium album, the only chemoorganotrophic member of the phylumChlorobi. New genus and speciesMelioribacter roseusare proposed for isolateP3M‐2T. Together withI. album, the new organism represents the classIgnavibacteriaassigned to the phylumChlorobi. The revealed group includes a variety of uncultured environmental clones, the16S rRNAgene sequences of some of which have been previously attributed to the candidate divisionZB1. Phylogenetic analysis ofM. roseusandI. albumbased on their23S rRNAandRecAsequences confirmed that these two organisms could represent an even deeper, phylum‐level lineage. Hence, we propose a new phylumIgnavibacteriaewithin theBacteroidetes–Chlorobigroup with a sole classIgnavibacteria, two familiesIgnavibacteriaceaeandMelioribacteraceaeand two speciesI. albumandM. roseus. This proposal correlates with chemotaxonomic data and phenotypic differences of both organisms from other cultured representatives ofChlorobi. The most essential differences, supported by the analyses of complete genomes of both organisms, are motility, facultatively anaerobic and obligately organotrophic mode of life, the absence of chlorosomes and the apparent inability to grow phototrophically.