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

Research output: Contribution to journalArticlepeer-review

276 Scopus citations

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.

Original languageEnglish (US)
Pages (from-to)22169-22174
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume106
Issue number52
DOIs
StatePublished - Dec 19 2009

All Science Journal Classification (ASJC) codes

  • General

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