JB Accepts, published online ahead of print on 6 November 2009

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J. Bacteriol. doi:10.1128/JB.00925-09
Copyright (c) 2009, American Society for Microbiology and/or the Listed Authors/Institutions. All Rights Reserved.

The Mtr Respiratory Pathway is Essential for Reducing Flavins and Electrodes in Shewanella oneidensis

Dan Coursolle, Daniel B. Baron, Daniel R. Bond, and Jeffery A. Gralnick^*

BioTechnology Institute and Department of Microbiology, University of Minnesota-Twin Cities, St. Paul, MN 55108

^* To whom correspondence should be addressed. Email: gralnick{at}umn.edu.

The Mtr respiratory pathway of Shewanella oneidensis strain MR-1 is required to effectively respire both soluble and insoluble forms of oxidized iron. Flavins (riboflavin and flavin mononucleotide) have recently been shown to be excreted by MR-1 and facilitate reduction of insoluble substrates. Other Shewanella species tested accumulated flavins in supernatants to a similar extent as MR-1, suggesting that flavin secretion is a general trait of the species. External flavins have been proposed act as both a soluble electron shuttle and a metal chelator, however at biologically relevant concentrations our results suggest that external flavins primarily act as electron shuttles for MR-1. Using deletion mutants lacking various Mtr-associated proteins, we demonstrate that the Mtr extracellular respiratory pathway is essential for reduction of flavins and that decaheme cytochromes found on the outer surface of the cell (MtrC and OmcA) are required for the majority of this activity. Given the involvement of external flavins in reduction of electrodes, we monitored current production by Mtr respiratory pathway mutants in three-electrode bioreactors under controlled flavin concentrations. While mutants lacking MtrC were able to reduce flavins at 50% the rate of wild type in cell suspension assays, these strains were unable to grow into productive electrode-reducing biofilms. Analysis of mutants lacking OmcA suggests a role for this protein in both electron transfer to electrodes and attachment to surfaces. The parallel phenotypes of Mtr mutants in flavin and electrode reduction blur the distinction between direct contact and redox shuttling strategies of insoluble substrate reduction by MR-1.