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

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,...

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Main Authors: Cornforth, Daniel M., Popat, Roman, McNally, Luke, Gurney, James, Scott-Phillips, Thomas C., Ivens, Alasdair, Diggle, Stephen P., Brown, Sam P.
Format: Article
Published: National Academy of Sciences 2014
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Online Access:https://eprints.nottingham.ac.uk/35961/
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author Cornforth, Daniel M.
Popat, Roman
McNally, Luke
Gurney, James
Scott-Phillips, Thomas C.
Ivens, Alasdair
Diggle, Stephen P.
Brown, Sam P.
author_facet Cornforth, Daniel M.
Popat, Roman
McNally, Luke
Gurney, James
Scott-Phillips, Thomas C.
Ivens, Alasdair
Diggle, Stephen P.
Brown, Sam P.
author_sort Cornforth, Daniel M.
building Nottingham Research Data Repository
collection Online Access
description 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.
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spelling nottingham-359612020-05-04T16:45:26Z https://eprints.nottingham.ac.uk/35961/ 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. 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. National Academy of Sciences 2014-03-05 Article PeerReviewed Cornforth, Daniel M., Popat, Roman, McNally, Luke, Gurney, James, Scott-Phillips, Thomas C., Ivens, Alasdair, Diggle, Stephen P. and Brown, Sam P. (2014) Combinatorial quorum sensing allows bacteria to resolve their social and physical environment. Proceedings of the National Academy of Sciences, 111 (11). pp. 4280-4284. ISSN 1091-6490 Diffusion Sensing Bacterial Signaling Efficiency Sensing Collective Behavior Bacterial Cooperation http://www.pnas.org/content/111/11/4280 doi:10.1073/pnas.1319175111 doi:10.1073/pnas.1319175111
spellingShingle Diffusion Sensing
Bacterial Signaling
Efficiency Sensing
Collective Behavior
Bacterial Cooperation
Cornforth, Daniel M.
Popat, Roman
McNally, Luke
Gurney, James
Scott-Phillips, Thomas C.
Ivens, Alasdair
Diggle, Stephen P.
Brown, Sam P.
Combinatorial quorum sensing allows bacteria to resolve their social and physical environment
title Combinatorial quorum sensing allows bacteria to resolve their social and physical environment
title_full Combinatorial quorum sensing allows bacteria to resolve their social and physical environment
title_fullStr Combinatorial quorum sensing allows bacteria to resolve their social and physical environment
title_full_unstemmed Combinatorial quorum sensing allows bacteria to resolve their social and physical environment
title_short Combinatorial quorum sensing allows bacteria to resolve their social and physical environment
title_sort combinatorial quorum sensing allows bacteria to resolve their social and physical environment
topic Diffusion Sensing
Bacterial Signaling
Efficiency Sensing
Collective Behavior
Bacterial Cooperation
url https://eprints.nottingham.ac.uk/35961/
https://eprints.nottingham.ac.uk/35961/
https://eprints.nottingham.ac.uk/35961/