Rapid electron exchange between surface-exposed bacterial cytochromes and Fe(III) minerals

• DOI: 10.1073/pnas.1220074110
• Publication Date: 2013-03-29T04:55:43Z
• Authors: Gaye F. White; Zhi Shi; Liang Shi; Zheming Wang; Alice C. Dohnalkova; Matthew J. Marshall; James K. Fredrickson; John M. Zachara; Julea N. Butt; David J. Richardson; Thomas A. Clarke
• Keywords: Models, Molecular; 0301 basic medicine; Shewanella; Immunoblotting; Molecular Sequence Data; 500; Cytochrome c Group; Molecular Sequence Annotation; Ferric Compounds; Electron Transport; 03 medical and health sciences; Bacterial Proteins; Multiprotein Complexes; Cytochromes; ATP-Binding Cassette Transporters; Amino Acid Sequence; Bacterial Outer Membrane Proteins

The mineral-respiring bacterium Shewanella oneidensis uses a protein complex, MtrCAB, composed of two decaheme cytochromes, MtrC and MtrA, brought together inside a transmembrane porin, MtrB, to transport electrons across the outer membrane to a variety of mineral-based electron acceptors. A proteoliposome system containing a pool of internalized electron carriers was used to investigate how the topology of the MtrCAB complex relates to its ability to transport electrons across a lipid bilayer to externally located Fe(III) oxides. With MtrA facing the interior and MtrC exposed on the outer surface of the phospholipid bilayer, the established in vivo orientation, electron transfer from the interior electron carrier pool through MtrCAB to solid-phase Fe(III) oxides was demonstrated. The rates were 10 3 times higher than those reported for reduction of goethite, hematite, and lepidocrocite by S. oneidensis , and the order of the reaction rates was consistent with those observed in S. oneidensis cultures. In contrast, established rates for single turnover reactions between purified MtrC and Fe(III) oxides were 10 3 times lower. By providing a continuous flow of electrons, the proteoliposome experiments demonstrate that conduction through MtrCAB directly to Fe(III) oxides is sufficient to support in vivo, anaerobic, solid-phase iron respiration.