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Extracellular DNA Promotes Efficient Extracellular Electron Transfer by Pyocyanin in Pseudomonas aeruginosa Biofilms

Saunders, Scott H. and Tse, Edmund C. M. and Yates, Matthew D. and Jiménez Otero, Fernanda and Trammell, Scott A. and Stemp, Eric D. A. and Barton, Jacqueline K. and Tender, Leonard M. and Newman, Dianne K. (2020) Extracellular DNA Promotes Efficient Extracellular Electron Transfer by Pyocyanin in Pseudomonas aeruginosa Biofilms. Cell, 182 (4). pp. 919-932. ISSN 0092-8674. PMCID PMC7457544. https://resolver.caltech.edu/CaltechAUTHORS:20191213-144717393

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1016/j.cell.2020.07.006DOIArticle
https://doi.org/10.1101/2019.12.12.872085DOIDiscussion Paper
ORCID:
AuthorORCID
Saunders, Scott H.0000-0003-4224-9106
Tse, Edmund C. M.0000-0002-9313-1290
Yates, Matthew D.0000-0003-4373-3864
Jiménez Otero, Fernanda0000-0003-1583-6495
Trammell, Scott A.0000-0002-7996-590X
Stemp, Eric D. A.0000-0003-2098-4214
Barton, Jacqueline K.0000-0001-9883-1600
Tender, Leonard M.0000-0001-8784-991X
Newman, Dianne K.0000-0003-1647-1918
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.
Group:Caltech Center for Environmental Microbial Interactions (CEMI), Rosen Bioengineering Center
Funders:
Funding AgencyGrant Number
NIH1R01AI127850-01A1
NIHGM126904
Army Research Office (ARO)W911NF-17-1-0024
Office of Naval Research (ONR)N0001418WX00436
Donna and Benjamin M. Rosen Bioengineering CenterUNSPECIFIED
Croucher FoundationUNSPECIFIED
Subject Keywords:biofilm; phenazine; extracellular electron transfer; Pseudomonas aeruginosa; pyocyanin; extracellular DNA; biofilm matrix; bacterial metabolism; DNA charge transfer
Issue or Number:4
PubMed Central ID:PMC7457544
Record Number:CaltechAUTHORS:20191213-144717393
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191213-144717393
Official Citation: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, Extracellular DNA Promotes Efficient Extracellular Electron Transfer by Pyocyanin in Pseudomonas aeruginosa Biofilms, Cell, Volume 182, Issue 4, 2020, Pages 919-932.e19, ISSN 0092-8674, https://doi.org/10.1016/j.cell.2020.07.006.
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:100293
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:16 Dec 2019 16:40
Last Modified:24 Nov 2020 20:39

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