Extracellular DNA Promotes Efficient Extracellular Electron Transfer by Pyocyanin in Pseudomonas aeruginosa Biofilms
Creators
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1.
California Institute of Technology
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2.
University of Hong Kong
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3.
United States Naval Research Laboratory
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4.
George Mason University
Abstract
Redox cycling of extracellular electron shuttles can enable the metabolic activity of subpopulations within multicellular bacterial biofilms that lack direct access to electron acceptors or donors. How these shuttles catalyze extracellular electron transfer (EET) within biofilms without being lost to the environment has been a long-standing question. Here, we show that phenazines mediate efficient EET through interactions with extracellular DNA (eDNA) in Pseudomonas aeruginosa biofilms. Retention of pyocyanin (PYO) and phenazine carboxamide in the biofilm matrix is facilitated by eDNA binding. In vitro, different phenazines can exchange electrons in the presence or absence of DNA and can participate directly in redox reactions through DNA. In vivo, biofilm eDNA can also support rapid electron transfer between redox active intercalators. Together, these results establish that PYO:eDNA interactions support an efficient redox cycle with rapid EET that is faster than the rate of PYO loss from the biofilm.
Additional Information
© 2020 Elsevier Inc. Received 12 December 2019, Revised 19 May 2020, Accepted 9 July 2020, Available online 6 August 2020. We thank Jeanyoung Jo, Lars Dietrich, and Matthew Parsek for providing strains and the Biological Imaging Center, GPS Division Analytical Facility, and Beckman Institute Laser Resource Center at Caltech for supporting confocal imaging, SEM imaging, and time resolved spectroscopy, respectively. We also thank three anonymous reviewers for their constructive comments. This work was supported by NIH (1R01AI127850-01A1 to D.K.N. and GM126904 to J.K.B.); ARO (W911NF-17-1-0024 to D.K.N.); ONR (N0001418WX00436 to M.D.Y., S.A.T., and L.M.T.); and Rosen Bioengineering Center at Caltech (to S.H.S., D.K.N., and J.K.B.). E.C.M.T. was supported by a Croucher Foundation Research Fellowship. Author Contributions: Conceptualization, S.H.S., J.K.B., L.M.T., and D.K.N.; Methodology, S.H.S., E.C.M.T., M.D.Y., F.J.O., S.A.T., E.D.A.S., J.K.B., L.M.T., and D.K.N.; Formal Analysis, S.H.S. and L.M.T.; Investigation, S.H.S., E.C.M.T., M.D.Y., F.J.O., S.A.T., and E.D.A.S.; Resources, J.K.B., L.M.T., and D.K.N.; Writing – Original Draft, S.H.S. and D.K.N.; Writing – Review & Editing, S.H.S., E.C.M.T., M.D.Y., F.J.O., S.A.T., E.D.A.S., J.K.B., L.M.T., and D.K.N.; Visualization, S.H.S.; Supervision, J.K.B., L.M.T., and D.K.N.; Funding Acquisition, J.K.B., L.M.T., and D.K.N. The authors declare no competing interests.Attached Files
Published - 1-s2.0-S0092867420308710-main.pdf
Submitted - 2019.12.12.872085v1.full.pdf
Supplemental Material - media-1.pdf
Files
1-s2.0-S0092867420308710-main.pdf
Additional details
Identifiers
- PMCID
- PMC7457544
- Eprint ID
- 100293
- Resolver ID
- CaltechAUTHORS:20191213-144717393
Related works
- Describes
- 10.1101/2019.12.12.872085 (DOI)
Funding
- NIH
- 1R01AI127850-01A1
- NIH
- GM126904
- Army Research Office (ARO)
- W911NF-17-1-0024
- Office of Naval Research (ONR)
- N0001418WX00436
- Donna and Benjamin M. Rosen Bioengineering Center
- Croucher Foundation
Dates
- Created
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2019-12-16Created from EPrint's datestamp field
- Updated
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2023-06-01Created from EPrint's last_modified field