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Journal of Bacteriology, July 2007, p. 4944-4952, Vol. 189, No. 13
0021-9193/07/$08.00+0     doi:10.1128/JB.01518-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Specific Bonds between an Iron Oxide Surface and Outer Membrane Cytochromes MtrC and OmcA from Shewanella oneidensis MR-1

Brian H. Lower,^1* Liang Shi,¹ Ruchirej Yongsunthon,² Timothy C. Droubay,¹ David E. McCready,¹ and Steven K. Lower²

Pacific Northwest National Laboratory, P.O. Box 999, Richland Washington 99352,¹ The Ohio State University, 125 South Oval Mall, 275 Mendenhall Laboratory, Columbus, Ohio 43210²

Received 28 September 2006/ Accepted 12 April 2007

Shewanella oneidensis MR-1 is purported to express outer membrane cytochromes (e.g., MtrC and OmcA) that transfer electrons directly to Fe(III) in a mineral during anaerobic respiration. A prerequisite for this type of reaction would be the formation of a stable bond between a cytochrome and an iron oxide surface. Atomic force microscopy (AFM) was used to detect whether a specific bond forms between a hematite (Fe₂O₃) thin film, created with oxygen plasma-assisted molecular beam epitaxy, and recombinant MtrC or OmcA molecules coupled to gold substrates. Force spectra displayed a unique force signature indicative of a specific bond between each cytochrome and the hematite surface. The strength of the OmcA-hematite bond was approximately twice that of the MtrC-hematite bond, but direct binding to hematite was twice as favorable for MtrC. Reversible folding/unfolding reactions were observed for mechanically denatured MtrC molecules bound to hematite. The force measurements for the hematite-cytochrome pairs were compared to spectra collected for an iron oxide and S. oneidensis under anaerobic conditions. There is a strong correlation between the whole-cell and pure-protein force spectra, suggesting that the unique binding attributes of each cytochrome complement one another and allow both MtrC and OmcA to play a prominent role in the transfer of electrons to Fe(III) in minerals. Finally, by comparing the magnitudes of binding force for the whole-cell versus pure-protein data, we were able to estimate that a single bacterium of S. oneidensis (2 by 0.5 µm) expresses 10⁴ cytochromes on its outer surface.

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* Corresponding author. Mailing address: Environmental Dynamics and Simulation Group, Pacific Northwest National Laboratory, P.O. Box 999, MS K8-96, Richland, WA 99352. Phone: (509) 376-6456. Fax: (509) 376-3650. E-mail: brian.lower{at}pnl.gov

Published ahead of print on 27 April 2007.

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Journal of Bacteriology, July 2007, p. 4944-4952, Vol. 189, No. 13
0021-9193/07/$08.00+0     doi:10.1128/JB.01518-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

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