Summary
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 Gammaproteobacteria. Metagenome assembly and binning revealed a novel betaproteobacterium, which we designate “Candidatus Dechloromonas occultata.” This organism dominated the enrichment and expressed a porin-cytochrome c complex typically associated with iron-oxidizing Betaproteobacteria and a novel cytochrome c-rich protein cluster (Occ), including an undecaheme putatively involved in extracellular electron transfer. 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.
Originality-significance Statement The prevalence of Mn(III)-ligand complexes in diverse aquatic environments is a recent geochemical discovery. Thus far, microbially-driven Mn(III) reduction has only been associated with Gammaproteobacteria encoding three-component outer-membrane porin-cytochrome c conduits. Here, we demonstrate that Betaproteobacteria dominate in abundance and protein expression during Mn(III) reduction in an enrichment culture. Using metaproteomics, we detect for the first time that Betaproteobacteria express a two-component porin-cytochrome c conduit, and an uncharacterized extracellular undecaheme c-type cytochrome. Although undecahemes have never been reported in Betaproteobacteria, we find that they are widespread in uncultivated strains. These results widen the phylogenetic diversity of Mn(III)-reducing bacteria, and provide new insights into potential molecular mechanisms for soluble Mn(III) reduction.
Footnotes
Changed title to broaden implications. Combined main text and supplemental text. Clarified that protein expression changes in bottles with methane could be due to lower redox potential.
