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

Gaye 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

Research output: Contribution to journalArticle

122 Citations (Scopus)

Abstract

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.
Original languageEnglish
Pages (from-to)6346-6351
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America (PNAS)
Volume110
Issue number16
Early online date28 Mar 2013
DOIs
Publication statusPublished - 16 Apr 2013

Keywords

  • cytochrome, mineral respiration, electron transfer

Cite this