Energy metabolism and multiple respiratory pathways revealed by genome sequencing of Desulfurispirillum indicum strain S5

Desulfurispirillum indicum strain S5, a novel obligate anaerobe belonging to the phylum Chrysiogenetes, is a dissimilatory selenate-, selenite-, arsenate-, nitrate- and nitrite-reducing bacterium. The circular genome of this metabolically versatile bacterium is 2.9Mbp, with a G+C content of 56.1% and 2619 predicted protein-coding genes. Genome analysis uncovered the components of the electron transport chain, providing important insights into the ability of D. indicum to adapt to different conditions, by coupling the oxidation of various electron donors to the reduction of a wide range of electron acceptors. Sequences encoding the subunits of dehydrogenases and enzymes with roles in the oxidation of several electron donors, including acetate, pyruvate and lactate were identified. Furthermore, five terminal oxidoreductase complexes were encoded in the D. indicum genome. Phylogenetic analyses of their catalytic subunits, operon structure and co-transcription of subunit-coding genes indicate a likely role of three of them as respiratory arsenate reductase (Arr), periplasmic nitrate reductase (Nap) and the membrane-bound nitrate reductase (Nar). This study is the first description and annotation of the genome of a dissimilatory selenate- and arsenate-respiring organism, and D. indicum represents the first sequenced member of its phylum. Our analysis demonstrates the complexity of the microorganism's respiratory system, provides the basis for the functional analysis of metalloid oxyanions respiration and expands our knowledge of the deep branching phylum of Chrysiogenetes.