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      The Fitness of Pseudomonas aeruginosa Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment

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          ABSTRACT

          Experiments examining the social dynamics of bacterial quorum sensing (QS) have focused on mutants which do not respond to signals and the role of QS-regulated exoproducts as public goods. The potential for QS signal molecules to themselves be social public goods has received much less attention. Here, we analyze how signal-deficient ( lasI) mutants of the opportunistic pathogen Pseudomonas aeruginosa interact with wild-type cells in an environment where QS is required for growth. We show that when growth requires a “private” intracellular metabolic mechanism activated by the presence of QS signal, lasI mutants act as social cheats and outcompete signal-producing wild-type bacteria in mixed cultures, because they can exploit the signals produced by wild-type cells. However, reducing the ability of signal molecules to diffuse through the growth medium results in signal molecules becoming less accessible to mutants, leading to reduced cheating. Our results indicate that QS signal molecules can be considered social public goods in a way that has been previously described for other exoproducts but that spatial structuring of populations reduces exploitation by noncooperative signal cheats.

          IMPORTANCE

          Bacteria communicate via signaling molecules to regulate the expression of a whole range of genes. This process, termed quorum sensing (QS), moderates bacterial metabolism under many environmental conditions, from soil and water (where QS-regulated genes influence nutrient cycling) to animal hosts (where QS-regulated genes determine pathogen virulence). Understanding the ecology of QS could therefore yield vital clues to how we might modify bacterial behavior for environmental or clinical gains. Here, we demonstrate that QS signals act as shareable public goods. This means that their evolution, and therefore population-level responses to interference with QS, will be constrained by population structure. Further, we show that environmental structure (constraints on signal diffusion) alters the accessibility of QS signals and demonstrates that we need to consider population and environmental structure to help us further our understanding of QS signaling systems.

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          Most cited references 47

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          Bacterial quorum sensing: its role in virulence and possibilities for its control.

          Quorum sensing is a process of cell-cell communication that allows bacteria to share information about cell density and adjust gene expression accordingly. This process enables bacteria to express energetically expensive processes as a collective only when the impact of those processes on the environment or on a host will be maximized. Among the many traits controlled by quorum sensing is the expression of virulence factors by pathogenic bacteria. Here we review the quorum-sensing circuits of Staphylococcus aureus, Bacillus cereus, Pseudomonas aeruginosa, and Vibrio cholerae. We outline these canonical quorum-sensing mechanisms and how each uniquely controls virulence factor production. Additionally, we examine recent efforts to inhibit quorum sensing in these pathogens with the goal of designing novel antimicrobial therapeutics.
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            Social evolution theory for microorganisms.

            Microorganisms communicate and cooperate to perform a wide range of multicellular behaviours, such as dispersal, nutrient acquisition, biofilm formation and quorum sensing. Microbiologists are rapidly gaining a greater understanding of the molecular mechanisms involved in these behaviours, and the underlying genetic regulation. Such behaviours are also interesting from the perspective of social evolution - why do microorganisms engage in these behaviours given that cooperative individuals can be exploited by selfish cheaters, who gain the benefit of cooperation without paying their share of the cost? There is great potential for interdisciplinary research in this fledgling field of sociomicrobiology, but a limiting factor is the lack of effective communication of social evolution theory to microbiologists. Here, we provide a conceptual overview of the different mechanisms through which cooperative behaviours can be stabilized, emphasizing the aspects most relevant to microorganisms, the novel problems that microorganisms pose and the new insights that can be gained from applying evolutionary theory to microorganisms.
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              Cooperation and conflict in quorum-sensing bacterial populations.

              It has been suggested that bacterial cells communicate by releasing and sensing small diffusible signal molecules in a process commonly known as quorum sensing (QS). It is generally assumed that QS is used to coordinate cooperative behaviours at the population level. However, evolutionary theory predicts that individuals who communicate and cooperate can be exploited. Here we examine the social evolution of QS experimentally in the opportunistic pathogen Pseudomonas aeruginosa, and show that although QS can provide a benefit at the group level, exploitative individuals can avoid the cost of producing the QS signal or of performing the cooperative behaviour that is coordinated by QS, and can therefore spread. We also show that a solution to the problem of exploitation is kin selection, if interacting bacterial cells tend to be close relatives. These results show that the problem of exploitation, which has been the focus of considerable attention in animal communication, also arises in bacteria.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                mBio
                MBio
                mbio
                mbio
                mBio
                mBio
                American Society for Microbiology (1752 N St., N.W., Washington, DC )
                2150-7511
                2 May 2017
                May-Jun 2017
                : 8
                : 3
                Affiliations
                [a ]Centre for Biomolecular Sciences, School of Life Sciences, University of Nottingham, Nottingham, United Kingdom
                [b ]Centre for Mathematics, Technical University of Munich (TUM), Garching, Germany
                [c ]School of Biological Sciences, Georgia Institute of Technology, Atlanta, Georgia, USA
                [d ]School of Life Sciences, University of Warwick, Coventry, United Kingdom
                University of Washington
                Author notes
                Address correspondence to Stephen P. Diggle, stephen.diggle@ 123456biosci.gatech.edu , or Freya Harrison, f.harrison@ 123456warwick.ac.uk .
                Article
                mBio00353-17
                10.1128/mBio.00353-17
                5414003
                28465424
                Copyright © 2017 Mund et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license.

                Page count
                supplementary-material: 5, Figures: 3, Tables: 0, Equations: 0, References: 45, Pages: 9, Words: 6089
                Product
                Funding
                Funded by: Deutsche Forschungsgemeinschaft (DFG) https://doi.org/10.13039/501100001659
                Award ID: Technical University of Munich Open Access Publishing Program
                Award Recipient : Anne Mund
                Funded by: Human Frontier Science Program (HFSP) https://doi.org/10.13039/501100000854
                Award ID: RGY0081/2012
                Award Recipient : Stephen P. Diggle
                Funded by: European Commission (EC) https://doi.org/10.13039/501100000780
                Award ID: Erasmus+ award
                Award Recipient : Anne Mund
                Funded by: RCUK | Natural Environment Research Council (NERC) https://doi.org/10.13039/501100000270
                Award ID: NE/J007064/1
                Award Recipient : Stephen P. Diggle
                Categories
                Research Article
                Custom metadata
                May/June 2017

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