Phenazine oxidation by a distal electrode modulates biofilm morphogenesis

Cornell, William Cole; Zhang, Yihan; Bendebury, Anastasia; Hartel, Andreas; Shepard, Kenneth L.; Dietrich, Lars E. P.

doi:10.1016/j.bioflm.2020.100025

Cited by 13 publications

(8 citation statements)

References 26 publications

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“…The bottom plot in Figure 5 C shows the charge profile of the five consecutive scans of this end point analysis and also indicates the CAT-PEG hydrogel contained more transferable electrons after it had been exposed to PYO Red -PEG hydrogel in the presence of the Ru 3+ -mediator. Consistent results using a slightly more oxidative mediator PMS ( Cornell et al., 2020b ) are shown in Figures S4 through S6 and discussed in the supplemental information .…”

Section: Resultssupporting

confidence: 78%

“…Importantly, much of redox-signaling occurs outside the cell and beyond the reach of typical biological control mechanisms, and thus this extracellular electron-flow appears to rely on spontaneous electron-transfer reactions. Two of the most important classes of bioorganics that can reversibly and spontaneously undergo redox reactions are phenolics (and especially catecholics) ( Fussell et al., 2011 ; Kim et al., 2019 ; Schweigert et al., 2001 ) and phenazines ( Cornell et al., 2020a ; Dietrich et al., 2008 ; Okegbe et al., 2012 ), and both are believed to be important in redox-signaling.…”

Section: Introductionmentioning

confidence: 99%

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Network-based redox communication between abiotic interactive materials

Zhao

Kim

et al. 2022

iScience

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Section: Resultssupporting

confidence: 78%

Section: Introductionmentioning

confidence: 99%

Network-based redox communication between abiotic interactive materials

Zhao

Kim

et al. 2022

iScience

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“…The intricate surface wrinkling patterns that we observe exclusively in exploring colonies may help cells respond to oxygen depletion by maximizing cell surface area for gas exchange. Indeed, increased colony wrinkling in response to oxygen depletion or impaired respiration appears to be a common response in microbial biofilm communities including those of Pseudomonas aeruginosa (31–33), Bacillus subtilis (34), Candida albicans (35), and Aspergillus fumigatus (36).…”

Section: Discussionmentioning

confidence: 99%

Exploratory growth in Streptomyces venezuelae involves a unique transcriptional program, enhanced oxidative stress response, and profound acceleration in response to glycerol

Shepherdson

Netzker

Stoyanov

et al. 2021

Preprint

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Exploration is a recently discovered mode of growth and behaviour exhibited by some Streptomyces species that is distinct from their classical sporulating life cycle. While much has been uncovered regarding initiating environmental conditions and the phenotypic outcomes of exploratory growth, how this process is coordinated at a genetic level remains unclear. We used RNA-sequencing to survey global changes in the transcriptional profile of exploring cultures over time in the model organism Streptomyces venezuelae. Transcriptomic analyses revealed widespread changes in gene expression impacting diverse cellular functions. Investigations into differentially expressed regulatory elements revealed specific groups of regulatory factors to be impacted, including the expression of several extracytoplasmic function (ECF) sigma factors, second messenger signalling pathways, and members of the whiB-like (wbl) family of transcription factors. Dramatic changes were observed among primary metabolic pathways, especially among respiration-associated genes and the oxidative stress response; enzyme assays confirmed that exploring cultures exhibit an enhanced oxidative stress response compared with classically growing cultures. Changes in expression of the glycerol catabolic genes in S. venezuelae led to the discovery that glycerol supplementation of the growth medium promotes a dramatic acceleration of exploration. This effect appears to be unique to glycerol as an alternative carbon source and this response is broadly conserved across other exploration-competent species.

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“…However, H2O2 has been known to prolong the wound healing process and is cytotoxic at high concentrations, which may be counteractive to its antimicrobial effects (12). Providing a poised electrode as alternative electron acceptor in the proximity of agar-grown P. aeruginosa PA14 colonies delays wrinkling colony morphology associated with the development of oxygen-limited regions by alleviating oxidant limitation (13). Additionally, biochemically altering PYO through demethylation has also been effective in decreasing P. aeruginosa PA14 cell survival and is synergistic with antibiotic treatment (14).…”

Section: Observationmentioning

confidence: 99%

Electrochemical disruption of extracellular electron transfer inhibits Pseudomonas aeruginosa cell survival within biofilms and is synergistic with antibiotic treatment

Otero

Newman

Tender

2022

Preprint

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Survival of cells within oxygen-limited regions in Pseudomonas aeruginosa biofilms is enabled by using small redox active molecules as electron shuttles to access distal oxidants. This respiratory versatility makes P. aeruginosa biofilms common in chronic wound infections and recalcitrant to treatment. Here, we show that electrochemically controlling the redox state of these electron shuttles, specifically pyocyanin, can impact cell survival within anaerobic P. aeruginosa biofilms and can act synergistically with antibiotic treatment. We inhibited pyocyanin redox cycling under anoxic conditions by blocking its ability to be re-oxidized and thus serve as an electron shuttle via poising an electrode at a reductive potential that cannot regenerate oxidized pyocyanin (i.e. -400mV vs Ag/AgCl). This resulted in a decrease in CFUs within the biofilm of 100x compared to samples exposed to an electrode poised at an oxidizing potential that permits pyocyanin re-oxidation (i.e. +100mV vs Ag/AgCl). Phenazine-deficient Δphz* biofilms were not affected by the redox potential of the electrode, but were re-sensitized by adding pyocyanin. The effect of EET disruption was exacerbated when biofilms were treated with sub-MICs of a range of antibiotics. Most notably, 4 μg/ml of the aminoglycoside gentamicin in a reductive environment almost completely eradicated wild type biofilms but had no effect on the survival of Δphz* biofilms, suggesting reduced phenazines are toxic, and combined with antibiotic treatment can lead to extensive killing.

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Phenazine oxidation by a distal electrode modulates biofilm morphogenesis

Cited by 13 publications

References 26 publications

Network-based redox communication between abiotic interactive materials

Network-based redox communication between abiotic interactive materials

Exploratory growth in Streptomyces venezuelae involves a unique transcriptional program, enhanced oxidative stress response, and profound acceleration in response to glycerol

Electrochemical disruption of extracellular electron transfer inhibits Pseudomonas aeruginosa cell survival within biofilms and is synergistic with antibiotic treatment

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