A novel uncultured bacterium of the family Gallionellaceae: Description and genome reconstruction based on metagenomic analysis of microbial community in acid mine drainage

Drainage waters at the metal mining areas often have low pH and high content of dissolved metals due to oxidation of sulfide minerals. Extreme conditions limit microbial diversity in such habitats. A microbial community of cold acid mine drainage (6.5°C, pH 2.65) at the Sherlovaya Gora polymetallic open-cast mine (Transbaikal region, Eastern Siberia, Russia) was studied using metagenomic techniques. Most of microorganisms belonged to a single uncultured lineage representing a new species of the Betaproteobacteria genus Gallionella. Bacteria of the genera Thiobacillus, Acidobacterium, Acidisphaera, and Acidithiobacillus were the minor components of the community. Almost complete (3.4 Mb) composite genome of the new bacterial lineage designated Candidatus Gallionella acididurans ShG14-8 was reconstructed using metagenomic data. Genome analysis revealed that Fe(II) oxidation probably involved the cytochromes localized on the outer cell membrane. The electron transport chain included NADH dehydrogenase, a cytochrome bc1 complex, an alternative complex III, and bd-, cbb3-, and bo3-types cytochrome oxidases. Oxidation of reduced sulfur compounds probably involved the Sox system, sulfide–quinone oxidoreductase, adenyl sulfate reductase, and sulfate adenyltransferase. The genes involved in autotrophic carbon assimilation via the Calvin cycle were present, while no pathway for nitrogen fixation was revealed. High numbers of RND metal transporters and P type ATPases were probably responsible for resistance to heavy metals. The new microorganism was an aerobic chemolithoautotroph that belonged to the group of psychrotolerant iron- and sulfur-oxidizing acidophiles of the family Gallionellaceae, which are widely distributed in acid mine drainage.