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Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms

View ORCID ProfileScott H. Saunders, View ORCID ProfileEdmund C.M. Tse, View ORCID ProfileMatthew D. Yates, View ORCID ProfileFernanda Jiménez Otero, View ORCID ProfileScott A. Trammell, View ORCID ProfileEric D.A. Stemp, View ORCID ProfileJacqueline K. Barton, View ORCID ProfileLeonard M. Tender, View ORCID ProfileDianne K. Newman
doi: https://doi.org/10.1101/2019.12.12.872085
Scott H. Saunders
1Division of Biology and Biological Engineering, Caltech, Pasadena, CA
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Edmund C.M. Tse
2Division of Chemistry and Chemical Engineering, Caltech, Pasadena, CA
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Matthew D. Yates
3Center for Bio/Molecular Science and Engineering, Naval Research Laboratory, Washington, DC
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Fernanda Jiménez Otero
4George Mason University, Fairfax, VA
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Scott A. Trammell
3Center for Bio/Molecular Science and Engineering, Naval Research Laboratory, Washington, DC
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Eric D.A. Stemp
5Department of Physical Sciences, Mt. Saint Mary’s University, Los Angeles, CA
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Jacqueline K. Barton
2Division of Chemistry and Chemical Engineering, Caltech, Pasadena, CA
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  • ORCID record for Jacqueline K. Barton
  • For correspondence: jkbarton@caltech.edu leonard.tender@nrl.navy.mil dkn@caltech.edu
Leonard M. Tender
3Center for Bio/Molecular Science and Engineering, Naval Research Laboratory, Washington, DC
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  • For correspondence: jkbarton@caltech.edu leonard.tender@nrl.navy.mil dkn@caltech.edu
Dianne K. Newman
1Division of Biology and Biological Engineering, Caltech, Pasadena, CA
6Division of Geological and Planetary Sciences, Caltech, Pasadena, CA
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  • For correspondence: jkbarton@caltech.edu leonard.tender@nrl.navy.mil dkn@caltech.edu
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SUMMARY

Extracellular electron transfer (EET), the process whereby cells access electron acceptors or donors that reside many cell lengths away, enables metabolic activity by microorganisms, particularly under oxidant-limited conditions that occur in multicellular bacterial biofilms. Although different mechanisms underpin this process in select organisms, a widespread strategy involves extracellular electron shuttles, redox-active metabolites that are secreted and recycled by diverse bacteria. How these shuttles catalyze electron transfer within biofilms without being lost to the environment has been a long-standing question. Here, we show that phenazine electron shuttles mediate efficient EET through interactions with extracellular DNA (eDNA) in Pseudomonas aeruginosa biofilms, which are important in nature and disease. Retention of pyocyanin (PYO) and phenazine carboxamide in the biofilm matrix is facilitated by binding to eDNA. In vitro, different phenazines can exchange electrons in the presence or absence of DNA and phenazines can participate directly in redox reactions through DNA; the biofilm eDNA can also support rapid electron transfer between redox active intercalators. Electrochemical measurements of biofilms indicate that retained PYO supports an efficient redox cycle with rapid EET and slow loss from the biofilm. Together, these results establish that eDNA facilitates phenazine metabolic processes in P. aeruginosa biofilms, suggesting a model for how extracellular electron shuttles achieve retention and efficient EET in biofilms.

Footnotes

  • https://github.com/DKN-lab/phz_eDNA_2019

  • https://DKN-lab.github.io/phz_eDNA_2019

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms
Scott H. Saunders, Edmund C.M. Tse, Matthew D. Yates, Fernanda Jiménez Otero, Scott A. Trammell, Eric D.A. Stemp, Jacqueline K. Barton, Leonard M. Tender, Dianne K. Newman
bioRxiv 2019.12.12.872085; doi: https://doi.org/10.1101/2019.12.12.872085
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Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms
Scott H. Saunders, Edmund C.M. Tse, Matthew D. Yates, Fernanda Jiménez Otero, Scott A. Trammell, Eric D.A. Stemp, Jacqueline K. Barton, Leonard M. Tender, Dianne K. Newman
bioRxiv 2019.12.12.872085; doi: https://doi.org/10.1101/2019.12.12.872085

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