Diffusion-Based Recycling of Flavins Allows Shewanella oneidensis MR-1 To Yield Energy from Metal Reduction Across Physical Separations

We fabricated a microfluidic reactor with a nanoporous barrier to characterize electron transport between Shewanella oneidensis MR-1 and the metal oxide birnessite across a physical separation. Real-time quantification of electron flux across this barrier by strains with different electron transfer capabilities revealed that this bacterium exports flavins to its surroundings when faced with no direct physical access to an electron acceptor, allowing it to reduce metals at distances exceeding 60 mu m. An energy balance indicates that flavins must be recycled for S. oneidensis MR-1 to yield energy from lactate oxidation coupled to flavin reduction. In our system, we find that flavins are recycled between 24 and 60 times depending on flow conditions. This energy saving strategy, which until now had not been systematically tested or captured in environmentally relevant systems, suggests that electron shuttling microorganisms have the capacity to access and reduce metals in physically distant or potentially toxic microenvironments (i.e., pores with soluble and transiently sorbed toxins) where direct contact is limited or unfavorable. Our results challenge the prediction that diffusion-based electron shuttling is only effective across short distances and may lead to improved bioremediation strategies or advance biogeochemical models of electron transfer in anaerobic sediments.