Fe(III) Oxide Reduction Bypassing Outer-Surface Cytochromes in a Marine Respiratory Anaerobe

Microbial Fe(III) oxide reduction is a key process controlling carbon turnover and redox chemistry in anaerobic soils and sediments. Yet the mechanisms of extracellular electron transfer (EET) that govern the effectiveness of microbes accessing Fe(III) oxides remain poorly understood. Most mechanistic insights are derived from just two freshwater isolates. Therefore, we evaluated the EET mechanisms of Desulfovibrio ferrophilus, as a model for Fe(III) oxide reduction in marine sediments. Although D. ferrophilus grew with Fe(III) oxide as the sole electron acceptor, washed cell suspensions failed to reduce Fe(III), despite the expression of multiple outer-surface c-type cytochromes homologous to proteins previously implicated in EET. Deletion of these cytochrome genes did not impair growth on Fe(III) oxide. Cultures produced 2-amino-3-carboxy-1,4-naphthoquinone (ACNQ), a soluble electron shuttle that enabled EET activity when added to cell suspensions. These results demonstrate that respiratory Fe(III) reducers can rely on internally reduced electron shuttles even when expressing outer-surface cytochromes. This previously unrecognized mechanism for Fe(III) oxide reduction in a respiratory anaerobe that is abundant in sedimentary environments provides a key concept for improving biogeochemical models and for interpreting extracellular electron transfer mechanisms inferred from omics-based studies of anaerobic ecosystems.