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Phenazine oxidation by a distal electrode modulates biofilm morphogenesis.

ABSTRACT: Microbes living in biofilms, dense assemblages of cells, experience limitation for resources such as oxygen when cellular consumption outpaces diffusion. The pathogenic bacterium Pseudomonas aeruginosa has strategies for coping with hypoxia that support cellular redox balancing in biofilms; these include (1) increasing access to oxygen by forming wrinkles in the biofilm surface and (2) electrochemically reducing endogenous compounds called phenazines, which can shuttle electrons to oxidants available at a distance. Phenazine-mediated extracellular electron transfer (EET) has been shown to support survival for P. aeruginosa cells in anoxic liquid cultures, but the physiological relevance of EET over a distance for P. aeruginosa biofilms has remained unconfirmed. Here, we use a custom-built electrochemistry setup to show that phenazine-mediated electron transfer at a distance inhibits wrinkle formation in P. aeruginosa biofilms. This result demonstrates that phenazine-dependent EET to a distal oxidant affects biofilm morphogenesis.

SUBMITTER: Cornell WC

PROVIDER: S-EPMC7798475 | biostudies-literature | 2020 Dec

REPOSITORIES: biostudies-literature

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Phenazine oxidation by a distal electrode modulates biofilm morphogenesis.

Cornell William Cole WC Zhang Yihan Y Bendebury Anastasia A Hartel Andreas J W AJW Shepard Kenneth L KL Dietrich Lars E P LEP

Biofilm 20200513

Microbes living in biofilms, dense assemblages of cells, experience limitation for resources such as oxygen when cellular consumption outpaces diffusion. The pathogenic bacterium <i>Pseudomonas aeruginosa</i> has strategies for coping with hypoxia that support cellular redox balancing in biofilms; these include (1) increasing access to oxygen by forming wrinkles in the biofilm surface and (2) electrochemically reducing endogenous compounds called phenazines, which can shuttle electrons to oxidan ...[more]

PMID: 33447810

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Project description:Within biofilms, gradients of electron acceptors such as oxygen stimulate the formation of physiological subpopulations. This heterogeneity can enable cross-feeding and promote drug resilience, features of the multicellular lifestyle that make biofilm-based infections difficult to treat. The pathogenic bacterium Pseudomonas aeruginosa produces pigments called phenazines that can support metabolic activity in hypoxic/anoxic biofilm subzones, but these compounds also include methylated derivatives that are toxic to their producer under some conditions. Here, we uncover roles for the global regulators RpoS and Hfq/Crc in controlling the beneficial and detrimental effects of methylated phenazines in biofilms. Our results indicate that RpoS controls phenazine methylation by modulating activity of the carbon catabolite repression pathway, in which the Hfq/Crc complex inhibits translation of the phenazine methyltransferase PhzM. We find that RpoS indirectly inhibits expression of CrcZ, a small RNA that binds to and sequesters Hfq/Crc, specifically in the oxic subzone of P. aeruginosa biofilms. Deletion of rpoS or crc therefore leads to overproduction of methylated phenazines, which we show leads to increased metabolic activity-an apparent beneficial effect-in hypoxic/anoxic subpopulations within biofilms. However, we also find that biofilms lacking Crc show increased sensitivity to an exogenously added methylated phenazine, indicating that the increased metabolic activity in this mutant comes at a cost. Together, these results suggest that complex regulation of PhzM allows P. aeruginosa to simultaneously exploit the benefits and limit the toxic effects of methylated phenazines.Significance statementP. aeruginosa causes biofilm-based infections and is known for its production of colorful phenazine derivatives. Among these the methylated phenazines are the most toxic and can cause condition-dependent damage to their producer. In this study, we show that methylated phenazines also have a beneficial effect in that they specifically support metabolic activity at depth in P. aeruginosa biofilms, where oxygen limitation would otherwise stall metabolism. We describe a new link between P. aeruginosa global regulators that control methylated phenazine production in a manner that limits their toxicity while simultaneously enabling their contribution to metabolism. These results expand our understanding of the strategies that enable P. aeruginosa survival in multicellular structures, which is key to its success during chronic host colonization.

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Phenazine oxidation by a distal electrode modulates biofilm morphogenesis.

Publications

Phenazine oxidation by a distal electrode modulates biofilm morphogenesis.

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