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Research Article

Characterization of an electron conduit between bacteria and the extracellular environment

Robert S. Hartshorne, Catherine L. Reardon, Daniel Ross, Jochen Nuester, Thomas A. Clarke, Andrew J. Gates, Paul C. Mills, Jim K. Fredrickson, John M. Zachara, Liang Shi, Alex S. Beliaev, Matthew J. Marshall, Ming Tien, Susan Brantley, Julea N. Butt, and David J. Richardson
PNAS December 29, 2009 106 (52) 22169-22174; https://doi.org/10.1073/pnas.0900086106
Robert S. Hartshorne
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Catherine L. Reardon
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Daniel Ross
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Jochen Nuester
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Thomas A. Clarke
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Andrew J. Gates
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Paul C. Mills
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Jim K. Fredrickson
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John M. Zachara
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Liang Shi
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Alex S. Beliaev
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Matthew J. Marshall
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Ming Tien
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Susan Brantley
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Julea N. Butt
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David J. Richardson
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  • For correspondence: d.richardson@uea.ac.uk
  1. Edited by Dianne Newman, Massachusetts Institute of Technology, Cambridge, MA, and accepted by the Editorial Board September 9, 2009 (received for review January 7, 2009)

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Abstract

A number of species of Gram-negative bacteria can use insoluble minerals of Fe(III) and Mn(IV) as extracellular respiratory electron acceptors. In some species of Shewanella, deca-heme electron transfer proteins lie at the extracellular face of the outer membrane (OM), where they can interact with insoluble substrates. To reduce extracellular substrates, these redox proteins must be charged by the inner membrane/periplasmic electron transfer system. Here, we present a spectro-potentiometric characterization of a trans-OM icosa-heme complex, MtrCAB, and demonstrate its capacity to move electrons across a lipid bilayer after incorporation into proteoliposomes. We also show that a stable MtrAB subcomplex can assemble in the absence of MtrC; an MtrBC subcomplex is not assembled in the absence of MtrA; and MtrA is only associated to the membrane in cells when MtrB is present. We propose a model for the modular organization of the MtrCAB complex in which MtrC is an extracellular element that mediates electron transfer to extracellular substrates and MtrB is a trans-OM spanning β-barrel protein that serves as a sheath, within which MtrA and MtrC exchange electrons. We have identified the MtrAB module in a range of bacterial phyla, suggesting that it is widely used in electron exchange with the extracellular environment.

  • cytochrome-c
  • iron respiration
  • protein film voltammetry
  • electron paramagnetic resonance
  • Shewanella

Footnotes

  • 1To whom correspondence should be addressed. E-mail: d.richardson{at}uea.ac.uk
  • Author contributions: R.S.H., C.L.R., T.A.C., J.K.F., J.M.Z., L.S., A.S.B., M.J.M., M.T., S.B., J.N.B., and D.J.R. designed research; R.S.H., C.L.R., D.R., J.N., T.A.C., A.J.G., P.C.M., L.S., A.S.B., and M.J.M. performed research; R.S.H., C.L.R., D.R., J.N., T.A.C., A.J.G., and J.N.B. analyzed data; and T.A.C., J.K.F., J.M.Z., M.T., S.B., J.N.B., and D.J.R. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission. D.N. is a guest editor invited by the Editorial Board.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0900086106/DCSupplemental.

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Characterization of an electron conduit between bacteria and the extracellular environment
Robert S. Hartshorne, Catherine L. Reardon, Daniel Ross, Jochen Nuester, Thomas A. Clarke, Andrew J. Gates, Paul C. Mills, Jim K. Fredrickson, John M. Zachara, Liang Shi, Alex S. Beliaev, Matthew J. Marshall, Ming Tien, Susan Brantley, Julea N. Butt, David J. Richardson
Proceedings of the National Academy of Sciences Dec 2009, 106 (52) 22169-22174; DOI: 10.1073/pnas.0900086106

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Characterization of an electron conduit between bacteria and the extracellular environment
Robert S. Hartshorne, Catherine L. Reardon, Daniel Ross, Jochen Nuester, Thomas A. Clarke, Andrew J. Gates, Paul C. Mills, Jim K. Fredrickson, John M. Zachara, Liang Shi, Alex S. Beliaev, Matthew J. Marshall, Ming Tien, Susan Brantley, Julea N. Butt, David J. Richardson
Proceedings of the National Academy of Sciences Dec 2009, 106 (52) 22169-22174; DOI: 10.1073/pnas.0900086106
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