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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. (2019) Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms. . (Unpublished) https://resolver.caltech.edu/CaltechAUTHORS:20191213-144717393

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Abstract

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 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.


Item Type:Report or Paper (Discussion Paper)
Related URLs:
URLURL TypeDescription
https://doi.org/10.1101/2019.12.12.872085DOIDiscussion Paper
ORCID:
AuthorORCID
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: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. bioRxiv preprint first posted online Dec. 12, 2019. We thank Jeanyoung Jo, Lars Dietrich and Matthew Parsek for providing strains. This work was supported by grants to D.K.N. from NIH (1R01AI127850- 01A1) and ARO (W911NF-17-1-0024), to J.K.B. from NIH (GM126904), and to S.H.S., D.K.N and J.K.B. from the Rosen Bioengineering Center at Caltech. 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., 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., 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 – Reviewing & 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., 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. Authors declare no competing interests. Data and materials availability: Data and strains used in this study are available on request. Data and code are available at github.com/DKN-lab/phz_eDNA_2019.
Group:Caltech Center for Environmental Microbial Interactions (CEMI), Rosen Bioengineering Center
Funders:
Funding AgencyGrant Number
NIH1R01AI127850-01A1
Army Research Office (ARO)W911NF-17-1-0024
NIHGM126904
Donna and Benjamin M. Rosen Bioengineering CenterUNSPECIFIED
Record Number:CaltechAUTHORS:20191213-144717393
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20191213-144717393
Official Citation:Extracellular DNA promotes efficient extracellular electron transfer by pyocyanin in Pseudomonas aeruginosa biofilms Scott H. Saunders, Edmund C.M. Tse, Matthew D. Yates, Fernanda Jimenez 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
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:16 Dec 2019 16:40

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