Expression of extracellular multiheme cytochromes discovered in a betaproteobacterium during Mn(III) reduction

Soluble ligand-bound Mn(III) can support anaerobic microbial respiration in diverse aquatic environments. Thus far, Mn(III) reduction has only been associated with certain Gammaproteobacteria. Here, we characterized microbial communities enriched from Mn-replete sediments of Lake Matano, Indonesia. Our results provide the first evidence for biological reduction of soluble Mn(III) outside of the Gammaproteobacteria. Metagenome assembly and binning revealed a novel betaproteobacterium, which we designate "Candidatus Dechloromonas occultata". This organism dominated the enrichment and expressed a novel cytochrome c-rich protein cluster (Occ), including an undecaheme putatively involved in extracellular electron transfer during Mn(III) reduction. The occ gene cluster was detected in diverse aquatic bacteria, including uncultivated Betaproteobacteria from the deep subsurface. These observations provide new insight into the taxonomic and functional diversity of microbially-driven Mn(III) reduction in natural environments.