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

Molecular Microbiology
Nathaniel R GlasserDianne K Newman

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.

References

Apr 1, 1986·Infection and Immunity·C D Cox
Feb 1, 1968·Proceedings of the National Academy of Sciences of the United States of America·U HopferT E Thompson
Apr 1, 1983·Applied and Environmental Microbiology·C A Carlson, J L Ingraham
Dec 1, 1981·Antimicrobial Agents and Chemotherapy·S S Baron, J J Rowe
Oct 31, 1998·Applied and Environmental Microbiology·M BenzA Brune
Dec 26, 2001·Proceedings of the National Academy of Sciences of the United States of America·H G CalamitaR J Doyle
Dec 18, 2002·Journal of Bacteriology·Dieter WeichartRegine Hengge-Aronis
Jun 14, 2005·Trends in Microbiology·Gee W LauBradley E Britigan
Jul 21, 2005·Journal of Bacteriology·Kelli L PalmerMarvin Whiteley
Jan 20, 2006·Nature Chemical Biology·Alexa Price-WhelanDianne K Newman
Feb 16, 2006·Proceedings of the National Academy of Sciences of the United States of America·Nicole T LiberatiFrederick M Ausubel
May 25, 2006·Annual Review of Phytopathology·Dmitri V MavrodiLinda S Thomashow
Jul 6, 2006·Applied and Environmental Microbiology·Robert M Q ShanksGeorge A O'Toole
Sep 18, 2007·Journal of Bacteriology·Kelli L PalmerMarvin Whiteley
May 29, 2008·Environmental Science & Technology·Yun Wang, Dianne K Newman
Feb 17, 2009·Applied and Environmental Microbiology·Volker BehrendsJacob G Bundy
Jun 10, 2010·Annual Review of Microbiology·Kim Lewis
Jun 23, 2010·Proceedings of the National Academy of Sciences of the United States of America·Henrik Strahl, Leendert W Hamoen
Apr 6, 2011·Nature Reviews. Microbiology·Terry A KrulwichEtana Padan
May 13, 2011·Nature·Kyle R AllisonJames J Collins
Jun 16, 2011·ACS Chemical Biology·Nora L SullivanDianne Newman

❮ Previous
Next ❯

Citations

Jan 21, 2016·Proceedings of the National Academy of Sciences of the United States of America·Brett M BabinDavid A Tirrell
Apr 29, 2015·Frontiers in Microbiology·Simone SchmitzMiriam A Rosenbaum
Oct 12, 2014·Applied Microbiology and Biotechnology·Xilin DuYuquan Xu
Jun 9, 2016·Proceedings of the National Academy of Sciences of the United States of America·Hassan SakhtahLars E P Dietrich
Aug 12, 2016·Nature Reviews. Microbiology·Megan BergkesselDianne K Newman
Apr 20, 2016·Journal of Microbiological Methods·Sang-Jin SuhLaura Silo-Suh
Aug 19, 2015·Biotechnology and Bioengineering·Michaela A TerAvest, Caroline M Ajo-Franklin
Jan 18, 2017·Bioorganic & Medicinal Chemistry·Nikolaus GuttenbergerRolf Breinbauer
Jun 28, 2017·Annual Review of Biochemistry·Abigail J SporerLars E P Dietrich
Feb 6, 2018·FEMS Microbiology Letters·Serena RinaldoFrancesca Cutruzzolà
Jun 14, 2017·Proceedings of the National Academy of Sciences of the United States of America·Chinweike OkegbeLars E P Dietrich
Dec 1, 2017·MBio·Kieran B PechterCaroline S Harwood
Apr 21, 2018·Molecular Plant Pathology·Young Cheol Kim, Anne J Anderson
Feb 17, 2017·Environmental Microbiology·Kelley A GallagherPaul R Jensen
Jun 12, 2016·Applied and Environmental Microbiology·Erick M BosireMiriam A Rosenbaum
Aug 31, 2018·Environmental Microbiology·Adrien Biessy, Martin Filion
Sep 20, 2018·Molecular Microbiology·Lucas A Meirelles, Dianne K Newman
Jan 10, 2019·The Journal of Biological Chemistry·Emily M ZygielElizabeth M Nolan
Jul 22, 2017·Annual Review of Microbiology·Nathaniel R GlasserDianne K Newman
Sep 19, 2019·Journal of Bacteriology·Alex W CrockerDeborah A Hogan
Nov 27, 2019·Cellular and Molecular Life Sciences : CMLS·Heejoon ParkRoss P Carlson
Jan 11, 2017·Journal of Breath Research·Joann PhanKatrine Whiteson
Feb 20, 2020·Journal of Bacteriology·John A Ciemniecki, Dianne K Newman
Feb 23, 2019·Nature Reviews. Microbiology·Yinon M Bar-On, Ron Milo
Sep 16, 2020·Journal of Industrial Microbiology & Biotechnology·Dinesh GuptaArpita Bose
Aug 6, 2020·Frontiers in Microbiology·Eva Arrebola, Francisco M Cazorla
Mar 17, 2018·Journal of Industrial Microbiology & Biotechnology·R Cameron CoatesYasuo Yoshikuni
Apr 24, 2018·Monatshefte für chemie·Nikolaus GuttenbergerRolf Breinbauer

❮ Previous
Next ❯

Related Concepts

Related Feeds

Bacterial Respiration

This feed focuses on cellular respiration in bacteria, known as bacterial respiration. Discover the latest research here.

ATP Synthases

ATP synthases are enzymes located in the inner mitochondrial membrane that catalyze the synthesis of ATP during cellular respiration. Discover the latest research on ATP synthases here.