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Membrane vesicles traffic signals and facilitate group activities in a prokaryote

Abstract

Many bacteria use extracellular signals to communicate and coordinate social activities, a process referred to as quorum sensing1. Many quorum signals have significant hydrophobic character, and how these signals are trafficked between bacteria within a population is not understood. Here we show that the opportunistic human pathogen Pseudomonas aeruginosa packages the signalling molecule 2-heptyl-3-hydroxy-4-quinolone (pseudomonas quinolone signal; PQS)2 into membrane vesicles that serve to traffic this molecule within a population. Removal of these vesicles from the bacterial population halts cell–cell communication and inhibits PQS-controlled group behaviour. We also show that PQS actively mediates its own packaging and the packaging of other antimicrobial quinolines produced by P. aeruginosa into vesicles. These findings illustrate that a prokaryote possesses a signal trafficking system with features common to those used by higher organisms and outlines a novel mechanism for delivery of a signal critical for coordinating group behaviour in P. aeruginosa.

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Figure 1: Packaging of the P. aeruginosa signalling molecule PQS into MVs.
Figure 2: Analysis of antimicrobial quinolines from P. aeruginosa MVs using LC–MS and CID.
Figure 3: Biological activities of MVs.
Figure 4: Exogenous PQS stimulates P. aeruginosa MV formation and is packaged into MVs.
Figure 5: PQS-mediated gene regulation is not required for MV formation.

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Acknowledgements

We thank K. Jackson for LC–MS analysis; L. Rahme for the mvfR mutant; and the MGH-Parabiosys:NHLBI Program for Genomic applications, Massachusetts General Hospital and Harvard Medical School (http://pga.mgh.harvard.edu/cgi-bin/pa14/mutants/retrieve.cgi), for the pqsA mutant. This work was supported by a grant from the Oklahoma Center for the Advancement of Science and Technology.

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Correspondence to Marvin Whiteley.

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Supplementary Figure S1

Transmission electron micrograph of negatively-stained P. aeruginosa membrane vesicles. (PPT 168 kb)

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Mashburn, L., Whiteley, M. Membrane vesicles traffic signals and facilitate group activities in a prokaryote. Nature 437, 422–425 (2005). https://doi.org/10.1038/nature03925

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