Abstract

ABSTRACTThe opportunistic human pathogen Pseudomonas aeruginosa is known for exhibiting diverse forms of collective behaviors, like swarming motility and biofilm formation. Swarming in P. aeruginosa is a collective movement of the bacterial population over a semisolid surface, but specific swarming signals are not clear. We hypothesize that specific environmental signals induce swarming in P. aeruginosa. We show that under nutrient-limiting conditions, a low concentration of ethanol provides a strong ecological motivation for swarming in P. aeruginosa strain PA14. Ethanol serves as a signal and not a source of carbon under these conditions. Moreover, ethanol-driven swarming relies on the ability of the bacteria to metabolize ethanol to acetaldehyde using a periplasmic quinoprotein alcohol dehydrogenase, ExaA. We found that ErdR, an orphan response regulator linked to ethanol oxidation, is necessary for the transcriptional regulation of a cluster of 17 genes, including exaA, during swarm lag. Further, we show that P. aeruginosa displays characteristic foraging motility on a lawn of Cryptococcus neoformans, a yeast species, in a manner dependent on the ethanol dehydrogenase ErdR and on rhamnolipids. Finally, we show that ethanol, as a volatile, could induce swarming in P. aeruginosa at a distance, suggesting long-range spatial effects of ethanol as a signaling molecule.

Highlights

  • The opportunistic human pathogen Pseudomonas aeruginosa is known for exhibiting diverse forms of collective behaviors, like swarming motility and biofilm formation

  • To understand the extrinsic cues that induce swarming in P. aeruginosa populations, we sought to investigate the transcriptional response of bacteria during the swarm lag

  • Our analyses of the transcriptome of bacteria in the early and late phases of swarm lag uncovered the critical role of the periplasmic ethanol oxidation machinery controlled by the response regulator ErdR in P. aeruginosa swarming

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Summary

Introduction

The opportunistic human pathogen Pseudomonas aeruginosa is known for exhibiting diverse forms of collective behaviors, like swarming motility and biofilm formation. Swarming in P. aeruginosa is a collective movement of the bacterial population over a semisolid surface, but specific swarming signals are not clear. We demonstrate the importance of a specific environmental cue, ethanol, produced by many microbes, in inducing swarming in the P. aeruginosa population during starvation. On a semisolid nutritionally defined surface, the opportunistic human pathogen Pseudomonas aeruginosa exhibits a characteristic flagellum-driven locomotory social trait called swarming [3]. Specific environmental signals that serve as ecological motivations for swarming in bacteria remain a poorly understood facet of this form of collective behavior. Do specific environmental signals induce the formation and extension of tendrils, a characteristic of P. aeruginosa swarming? Broad or nutrient-specific starvation might be essential for bacteria to engage in swarming

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