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Research Article

Electrokinesis is a microbial behavior that requires extracellular electron transport

H. W. Harris, M. Y. El-Naggar, O. Bretschger, M. J. Ward, M. F. Romine, A. Y. Obraztsova, and K. H. Nealson
  1. aDepartment of Biological Sciences, University of Southern California, Los Angeles, CA 90089
  2. bDepartment of Physics and Astronomy, University of Southern California, Los Angeles, CA 90089
  3. cJ. Craig Venter Institute, San Diego, CA 92121
  4. dDepartment of Earth Sciences, University of Southern California, Los Angeles, CA 90089
  5. eEnvironmental and Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA 99352

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PNAS first published December 14, 2009; https://doi.org/10.1073/pnas.0907468107
H. W. Harris
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M. Y. El-Naggar
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O. Bretschger
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M. J. Ward
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M. F. Romine
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A. Y. Obraztsova
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K. H. Nealson
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  • For correspondence: knealson@usc.edu
  1. Edited by E. Peter Greenberg, University of Washington, Seattle, WA, and approved November 11, 2009 (received for review July 4, 2009)

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Abstract

We report a previously undescribed bacterial behavior termed electrokinesis. This behavior was initially observed as a dramatic increase in cell swimming speed during reduction of solid MnO2 particles by the dissimilatory metal-reducing bacterium Shewanella oneidensis MR-1. The same behavioral response was observed when cells were exposed to small positive applied potentials at the working electrode of a microelectrochemical cell and could be tuned by adjusting the potential on the working electrode. Electrokinesis was found to be different from both chemotaxis and galvanotaxis but was absent in mutants defective in electron transport to solid metal oxides. Using in situ video microscopy and cell tracking algorithms, we have quantified the response for different strains of Shewanella and shown that the response correlates with current-generating capacity in microbial fuel cells. The electrokinetic response was only exhibited by a subpopulation of cells closest to the MnO2 particles or electrodes. In contrast, the addition of 1 mM 9,10-anthraquinone-2,6-disulfonic acid, a soluble electron shuttle, led to increases in motility in the entire population. Electrokinesis is defined as a behavioral response that requires functional extracellular electron transport and that is observed as an increase in cell swimming speeds and lengthened paths of motion that occur in the proximity of a redox active mineral surface or the working electrode of an electrochemical cell.

  • bacteria
  • microbial fuel cells
  • motility
  • chemotaxis
  • galvanotaxis

Footnotes

  • 1To whom correspondence should be addressed: E-mail: knealson{at}usc.edu.
  • Author contributions: H.W.H., M.Y.E.-N., O.B., A.O., and K.N. designed research; H.W.H. and O.B. performed research; M.F.R. contributed new reagents/analytic tools; H.W.H., M.Y.E.-N., O.B., M.J.W., M.F.R., A.O., and K.N. analyzed data; and H.W.H., M.Y.E.-N., M.J.W., and K.N. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • This article contains supporting information online at www.pnas.org/cgi/content/full/0907468107/DCSupplemental.

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Electrokinesis is a microbial behavior that requires extracellular electron transport
H. W. Harris, M. Y. El-Naggar, O. Bretschger, M. J. Ward, M. F. Romine, A. Y. Obraztsova, K. H. Nealson
Proceedings of the National Academy of Sciences Dec 2009, 200907468; DOI: 10.1073/pnas.0907468107

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Electrokinesis is a microbial behavior that requires extracellular electron transport
H. W. Harris, M. Y. El-Naggar, O. Bretschger, M. J. Ward, M. F. Romine, A. Y. Obraztsova, K. H. Nealson
Proceedings of the National Academy of Sciences Dec 2009, 200907468; DOI: 10.1073/pnas.0907468107
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