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Combinatorial quorum sensing allows bacteria to resolve their social and physical environment

Cornforth, Daniel M.; Popat, Roman; McNally, Luke; Gurney, James; Scott-Phillips, Thomas C.; Ivens, Alasdair; Diggle, Stephen P.; Brown, Sam P.

Authors

Daniel M. Cornforth

Roman Popat

Luke McNally

James Gurney

Thomas C. Scott-Phillips

Alasdair Ivens

Stephen P. Diggle

Sam P. Brown



Abstract

Quorum sensing (QS) is a cell–cell communication system that controls gene expression in many bacterial species, mediated by diffusible signal molecules. Although the intracellular regulatory mechanisms of QS are often well-understood, the functional roles of QS remain controversial. In particular, the use of multiple signals by many bacterial species poses a serious challenge to current functional theories. Here, we address this challenge by showing that bacteria can use multiple QS signals to infer both their social (density) and physical (mass-transfer) environment. Analytical and evolutionary simulation models show that the detection of, and response to, complex social/physical contrasts requires multiple signals with distinct half-lives and combinatorial (nonadditive) responses to signal concentrations. We test these predictions using the opportunistic pathogen Pseudomonas aeruginosa and demonstrate significant differences in signal decay betweeallyn its two primary signal molecules, as well as diverse combinatorial responses to dual-signal inputs. QS is associated with the control of secreted factors, and we show that secretome genes are preferentially controlled by synergistic “AND-gate” responses to multiple signal inputs, ensuring the effective expression of secreted factors in high-density and low mass-transfer environments. Our results support a new functional hypothesis for the use of multiple signals and, more generally, show that bacteria are capable of combinatorial communication.

Citation

Cornforth, D. M., Popat, R., McNally, L., Gurney, J., Scott-Phillips, T. C., Ivens, A., …Brown, S. P. (2014). Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proceedings of the National Academy of Sciences, 111(11), https://doi.org/10.1073/pnas.1319175111

Journal Article Type Article
Acceptance Date Feb 5, 2014
Publication Date Mar 5, 2014
Deposit Date Aug 23, 2016
Publicly Available Date Aug 23, 2016
Journal Proceedings of the National Academy of Sciences
Print ISSN 0027-8424
Electronic ISSN 1091-6490
Publisher National Academy of Sciences
Peer Reviewed Peer Reviewed
Volume 111
Issue 11
DOI https://doi.org/10.1073/pnas.1319175111
Keywords Diffusion Sensing, Bacterial Signaling, Efficiency Sensing, Collective Behavior, Bacterial Cooperation
Public URL http://eprints.nottingham.ac.uk/id/eprint/35961
Publisher URL http://www.pnas.org/content/111/11/4280
Copyright Statement Copyright information regarding this work can be found at the following address: http://eprints.nottingh.../end_user_agreement.pdf

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Copyright Statement
Copyright information regarding this work can be found at the following address: http://eprints.nottingham.ac.uk/end_user_agreement.pdf





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