scholarly journals Endogenous Phenazine Antibiotics Promote Anaerobic Survival of Pseudomonas aeruginosa via Extracellular Electron Transfer

2009 ◽  
Vol 192 (1) ◽  
pp. 365-369 ◽  
Author(s):  
Yun Wang ◽  
Suzanne E. Kern ◽  
Dianne K. Newman

ABSTRACT Antibiotics are increasingly recognized as having other, important physiological functions for the cells that produce them. An example of this is the effect that phenazines have on signaling and community development for Pseudomonas aeruginosa (L. E. Dietrich, T. K. Teal, A. Price-Whelan, and D. K. Newman, Science 321:1203-1206, 2008). Here we show that phenazine-facilitated electron transfer to poised-potential electrodes promotes anaerobic survival but not growth of Pseudomonas aeruginosa PA14 under conditions of oxidant limitation. Other electron shuttles that are reduced but not made by PA14 do not facilitate survival, suggesting that the survival effect is specific to endogenous phenazines.

Author(s):  
Scott H. Saunders ◽  
Edmund C.M. Tse ◽  
Matthew D. Yates ◽  
Fernanda Jiménez Otero ◽  
Scott A. Trammell ◽  
...  

SUMMARYExtracellular 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 redox active 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.


Cell ◽  
2020 ◽  
Vol 182 (4) ◽  
pp. 919-932.e19 ◽  
Author(s):  
Scott H. Saunders ◽  
Edmund C.M. Tse ◽  
Matthew D. Yates ◽  
Fernanda Jiménez Otero ◽  
Scott A. Trammell ◽  
...  

2012 ◽  
Vol 78 (19) ◽  
pp. 6987-6995 ◽  
Author(s):  
Misha G. Mehta-Kolte ◽  
Daniel R. Bond

ABSTRACTThe current understanding of dissimilatory metal reduction is based primarily on isolates from the proteobacterial generaGeobacterandShewanella. However, environments undergoing active Fe(III) reduction often harbor less-well-studied phyla that are equally abundant. In this work, electrochemical techniques were used to analyze respiratory electron transfer by the only known Fe(III)-reducing representative of theAcidobacteria,Geothrix fermentans. In contrast to previously characterized metal-reducing bacteria, which typically reach maximal rates of respiration at electron acceptor potentials of 0 V versus standard hydrogen electrode (SHE),G. fermentansrequired potentials as high as 0.55 V to respire at its maximum rate. In addition,G. fermentanssecreted two different soluble redox-active electron shuttles with separate redox potentials (−0.2 V and 0.3 V). The compound with the lower midpoint potential, responsible for 20 to 30% of electron transfer activity, was riboflavin. The behavior of the higher-potential compound was consistent with hydrophilic UV-fluorescent molecules previously found inG. fermentanssupernatants. Both electron shuttles were also produced when cultures were grown with Fe(III), but not when fumarate was the electron acceptor. This study reveals thatGeothrixis able to take advantage of higher-redox-potential environments, demonstrates that secretion of flavin-based shuttles is not confined toShewanella, and points to the existence of high-potential-redox-active compounds involved in extracellular electron transfer. Based on differences between the respiratory strategies ofGeothrixandGeobacter, these two groups of bacteria could exist in distinctive environmental niches defined by redox potential.


mBio ◽  
2013 ◽  
Vol 4 (1) ◽  
Author(s):  
Nicholas J. Kotloski ◽  
Jeffrey A. Gralnick

ABSTRACT Shewanella oneidensis strain MR-1 is widely studied for its ability to respire a diverse array of soluble and insoluble electron acceptors. The ability to breathe insoluble substrates is defined as extracellular electron transfer and can occur via direct contact or by electron shuttling in S. oneidensis. To determine the contribution of flavin electron shuttles in extracellular electron transfer, a transposon mutagenesis screen was performed with S. oneidensis to identify mutants unable to secrete flavins. A multidrug and toxin efflux transporter encoded by SO_0702 was identified and renamed bfe (bacterial flavin adenine dinucleotide [FAD] exporter) based on phenotypic characterization. Deletion of bfe resulted in a severe decrease in extracellular flavins, while overexpression of bfe increased the concentration of extracellular flavins. Strains lacking bfe had no defect in reduction of soluble Fe(III), but these strains were deficient in the rate of insoluble Fe(III) oxide reduction, which was alleviated by the addition of exogenous flavins. To test a different insoluble electron acceptor, graphite electrode bioreactors were set up to measure current produced by wild-type S. oneidensis and the Δbfe mutant. With the same concentration of supplemented flavins, the two strains produced similar amounts of current. However, when exogenous flavins were not supplemented to bioreactors, bfe mutant strains produced significantly less current than the wild type. We have demonstrated that flavin electron shuttling accounts for ~75% of extracellular electron transfer to insoluble substrates by S. oneidensis and have identified the first FAD transporter in bacteria. IMPORTANCE Extracellular electron transfer by microbes is critical for the geochemical cycling of metals, bioremediation, and biocatalysis using electrodes. A controversy in the field was addressed by demonstrating that flavin electron shuttling, not direct electron transfer or nanowires, is the primary mechanism of extracellular electron transfer employed by the bacterium Shewanella oneidensis. We have identified a flavin adenine dinucleotide transporter conserved in all sequenced Shewanella species that facilitates export of flavin electron shuttles in S. oneidensis. Analysis of a strain that is unable to secrete flavins demonstrated that electron shuttling accounts for ~75% of the insoluble extracellular electron transfer capacity in S. oneidensis.


2020 ◽  
Author(s):  
luyan ma

<p>Microbial nanowires are nanofilaments that could offer an extracellular electron transfer (EET) pathway linking the bacterial respiratory chain to external surfaces, such as oxidized metals in the environment and engineered electrodes in renewable energy devices. Filaments proposed to function as nanowires have been reported in multiple bacteria, yet it remains largely unclear about the composition and electron transfer mechanism of bacterial nanowires. Pseudomonas aeruginosa is an environmental and electrochemically active bacterium. In this study, we found nanotube-like extracellular filaments in P. aeruginosa biofilms, which were bacterial membrane extensions similar to the nanowires reported in Shewanella oneidensis. Remarkably, conductive probe atomic force microscope showed measurable conductivity of these extracellular filaments, suggesting that they may function as nanowires in P. aeruginosa. Our results also indicated that the electron shuttle pyocyanin significantly affected the conductivity of P. aeruginosa nanowires, suggesting that the electron transfer mechanism of P. aeruginosa nanowires was different from S. oneidensis. Furthermore, factors that impact biofilm formation, such as flagella, type IV pili, and exopolysaccharides, were not essential for nanowires formation, while affect the formation and length of nanowires of P. aeruginosa. Taken together, this is the first report that investigated the role of electron shuttle on the conductivity of nanowires and factors that affected nanowires formation.</p>


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