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Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosa by facilitating generation of ATP and a proton-motive force

Glasser, Nathaniel R. and Kern, Suzanne E. and Newman, Dianne K. (2014) Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosa by facilitating generation of ATP and a proton-motive force. Molecular Microbiology, 92 (2). pp. 399-412. ISSN 0950-382X. http://resolver.caltech.edu/CaltechAUTHORS:20140401-104038513

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Abstract

While many studies have explored the growth of Pseudomonas aeruginosa, comparatively few have focused on its survival. Previously, we reported that endogenous phenazines support the anaerobic survival of P. aeruginosa, yet the physiological mechanism underpinning survival was unknown. Here, we demonstrate that phenazine redox cycling enables P. aeruginosa to oxidize glucose and pyruvate into acetate, which promotes survival by coupling acetate and ATP synthesis through the activity of acetate kinase. By measuring intracellular NAD(H) and ATP concentrations, we show that survival is correlated with ATP synthesis, which is tightly coupled to redox homeostasis during pyruvate fermentation but not during arginine fermentation. We also show that ATP hydrolysis is required to generate a proton-motive force using the ATP synthase complex during fermentation. Together, our results suggest that phenazines enable maintenance of the proton-motive force by promoting redox homeostasis and ATP synthesis. This work demonstrates the more general principle that extracellular redox-active molecules, such as phenazines, can broaden the metabolic versatility of microorganisms by facilitating energy generation.


Item Type:Article
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http://dx.doi.org/10.1111/mmi.12566DOIArticle
http://onlinelibrary.wiley.com/doi/10.1111/mmi.12566/abstractPublisherArticle
http://onlinelibrary.wiley.com/doi/10.1111/mmi.12566/suppinfoPublisherSupporting Information
Additional Information:© 2014 John Wiley & Sons Ltd. Article first published online: 19 March 2014; Accepted manuscript online: 25 February 2014 02:52AM EST; Manuscript Accepted: 22 February 2014. This work was supported by the Howard Hughes Medical Institute (HHMI). D.K.N. is an HHMI Investigator, and N.R.G. and S.E.K. were both supported by NSF graduate research fellowships. This work was supported in part by the National Research Service Award (T32GM07676) from the National Institute of General Medical Sciences. We thank Nathan Dalleska and the Environmental Analysis Center (Caltech) for help with metabolite analyses, Ron Grimm for help with electrodes, and Ian Booth and members of the Newman lab for helpful discussions. The authors declare no conflicts of interest.
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Funding AgencyGrant Number
Howard Hughes Medical Institute (HHMI)UNSPECIFIED
NSF Graduate Research FellowshipUNSPECIFIED
National Institute of General Medical SciencesT32GM07676
Record Number:CaltechAUTHORS:20140401-104038513
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20140401-104038513
Official Citation:Glasser, N. R., Kern, S. E. and Newman, D. K. (2014), Phenazine redox cycling enhances anaerobic survival in Pseudomonas aeruginosa by facilitating generation of ATP and a proton-motive force. Molecular Microbiology, 92: 399–412. doi: 10.1111/mmi.12566
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:44573
Collection:CaltechAUTHORS
Deposited By: Jason Perez
Deposited On:01 Apr 2014 20:17
Last Modified:12 Jun 2014 20:29

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