Fe(III) oxide respiration by a Desulfovibrio species lacking canonical outer-membrane electron transfer systems

Desulfovibrio species play an important role in the extracellular reduction of Fe(III) oxides and other metals in diverse environments, but their extracellular electron transfer (EET) mechanisms are poorly understood. We found that Desulfovibrio strain JY grew with H₂ or lactate as the electron donor and poorly crystalline Fe(III) oxide as the electron acceptor, demonstrating the capacity to conserve energy from Fe(III) respiration despite the absence of genes for porin-cytochrome conduits, outer-surface cytochromes, or electrically conductive pili. Washed cell suspensions reduced Fe(III) citrate at rates comparable to that of Shewanella oneidensis, demonstrating the ability to effectively reduce soluble extracellular electron acceptors at the cell surface. Strain JY reduced the extracellular electron shuttles anthraquinone-2,6-disulfonate (AQDS) and riboflavin, which stimulated Fe(III) oxide reduction. Culture filtrates accelerated Fe(III) oxide reduction, and the reduction of Fe(III) oxide sequestered within porous alginate beads confirmed the presence of a shuttle. Riboflavin accumulated during growth on Fe(III) oxide, and electrochemical analysis and flavin measurements indicated that it was the primary shuttle. Genes encoding homologs of the S. oneidensis flavin exporter Bfe were more highly expressed during Fe(III) oxide respiration than during sulfate reduction. These results demonstrate that Desulfovibrio strain JY conserves energy to support growth from Fe(III) oxide reduction with a self-produced flavin electron shuttle, but without the canonical outer-membrane c-type cytochromes typically associated with EET in gram-negative bacteria. The findings expand the known diversity of microbial Fe(III) oxide respiration mechanisms and suggest that current genome-based prediction methods may substantially underestimate the diversity of electroactive microorganisms in natural environments.IMPORTANCEFe(III) oxide reduction is an important biogeochemical process influencing the cycling of carbon, nutrients, trace metals, and contaminants in anaerobic soils and sediments. The capacity for Fe(III) oxide reduction is commonly inferred from the presence of genes encoding porin-cytochrome conduits and outer-surface c-type cytochromes. The finding that a gram-negative microbe lacking these components can conserve energy to support growth from the reduction of Fe(III) oxides suggests that there is a much broader diversity of microbes capable of extracellular electron transfer than is generally considered. Genome-based strategies for elucidating the distribution and activity of electroactive microbes need revision to accommodate the expanding understanding of the range of mechanisms for electron transfer to insoluble extracellular electron acceptors.