33
views
0
recommends
+1 Recommend
0 collections
    0
    shares
      • Record: found
      • Abstract: found
      • Article: found
      Is Open Access

      Bacterial cell‐to‐cell signaling promotes the evolution of resistance to parasitic bacteriophages

      research-article

      Read this article at

      Bookmark
          There is no author summary for this article yet. Authors can add summaries to their articles on ScienceOpen to make them more accessible to a non-specialist audience.

          Abstract

          The evolution of host–parasite interactions could be affected by intraspecies variation between different host and parasite genotypes. Here we studied how bacterial host cell‐to‐cell signaling affects the interaction with parasites using two bacteria‐specific viruses (bacteriophages) and the host bacterium Pseudomonas aeruginosa that communicates by secreting and responding to quorum sensing ( QS) signal molecules. We found that a QS‐signaling proficient strain was able to evolve higher levels of resistance to phages during a short‐term selection experiment. This was unlikely driven by demographic effects (mutation supply and encounter rates), as nonsignaling strains reached higher population densities in the absence of phages in our selective environment. Instead, the evolved nonsignaling strains suffered relatively higher growth reduction in the absence of the phage, which could have constrained the phage resistance evolution. Complementation experiments with synthetic signal molecules showed that the Pseudomonas quinolone signal ( PQS) improved the growth of nonsignaling bacteria in the presence of a phage, while the activation of las and rhl quorum sensing systems had no effect. Together, these results suggest that QS‐signaling can promote the evolution of phage resistance and that the loss of QS‐signaling could be costly in the presence of phages. Phage–bacteria interactions could therefore indirectly shape the evolution of intraspecies social interactions and PQS‐mediated virulence in P. aeruginosa.

          Related collections

          Most cited references32

          • Record: found
          • Abstract: found
          • Article: not found

          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.
            Bookmark
            • Record: found
            • Abstract: found
            • Article: not found

            Identification, timing, and signal specificity of Pseudomonas aeruginosa quorum-controlled genes: a transcriptome analysis.

            There are two interrelated acyl-homoserine lactone quorum-sensing-signaling systems in Pseudomonas aeruginosa. These systems, the LasR-LasI system and the RhlR-RhlI system, are global regulators of gene expression. We performed a transcriptome analysis to identify quorum-sensing-controlled genes and to better understand quorum-sensing control of P. aeruginosa gene expression. We compared gene expression in a LasI-RhlI signal mutant grown with added signals to gene expression without added signals, and we compared a LasR-RhlR signal receptor mutant to its parent. In all, we identified 315 quorum-induced and 38 quorum-repressed genes, representing about 6% of the P. aeruginosa genome. The quorum-repressed genes were activated in the stationary phase in quorum-sensing mutants but were not activated in the parent strain. The analysis of quorum-induced genes suggests that the signal specificities are on a continuum and that the timing of gene expression is on a continuum (some genes are induced early in growth, most genes are induced at the transition from the logarithmic phase to the stationary phase, and some genes are induced during the stationary phase). In general, timing was not related to signal concentration. We suggest that the level of the signal receptor, LasR, is a critical trigger for quorum-activated gene expression. Acyl-homoserine lactone quorum sensing appears to be a system that allows ordered expression of hundreds of genes during P. aeruginosa growth in culture.
              Bookmark
              • Record: found
              • Abstract: found
              • Article: not found

              Quorum sensing and environmental adaptation in Pseudomonas aeruginosa: a tale of regulatory networks and multifunctional signal molecules.

              Bacteria employ sophisticated cell-to-cell communication or 'quorum sensing' (QS) systems for promoting collective behaviours that depend on the actions of one or more chemically distinct diffusible signal molecules. As determinants of cell population density, multiple QS systems are often integrated with each other and within global regulatory networks and subject to the prevailing environmental conditions as well as the presence and activities of other organisms. QS signal molecules, although largely considered as effectors of QS-dependent gene expression are also emerging as multifunctional molecules that influence life, development and death in single and mixed microbial populations and impact significantly the outcome of host-pathogen interactions.
                Bookmark

                Author and article information

                Contributors
                ville.friman@york.ac.uk
                Journal
                Ecol Evol
                Ecol Evol
                10.1002/(ISSN)2045-7758
                ECE3
                Ecology and Evolution
                John Wiley and Sons Inc. (Hoboken )
                2045-7758
                21 February 2017
                March 2017
                : 7
                : 6 ( doiID: 10.1002/ece3.2017.7.issue-6 )
                : 1936-1941
                Affiliations
                [ 1 ]Imperial College London, Silwood Park Campus Ascot BerkshireUK
                [ 2 ] School of Life Sciences Centre for Biomolecular SciencesUniversity of Nottingham NottinghamUK
                [ 3 ] Department of BiologyThe University of York YorkUK
                Author notes
                [*] [* ] Correspondence

                Ville‐Petri Friman, Department of Biology, The University of York, York, UK.

                Email: ville.friman@ 123456york.ac.uk

                Author information
                http://orcid.org/0000-0002-1592-157X
                Article
                ECE32818
                10.1002/ece3.2818
                5355186
                28331600
                fa0776e8-579a-4ed8-a05a-72da94edf81b
                © 2017 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 28 September 2016
                : 19 December 2016
                : 28 January 2017
                Page count
                Figures: 2, Tables: 0, Pages: 6, Words: 4525
                Funding
                Funded by: Wellcome Trust
                Award ID: 105624
                Funded by: Natural Environment Research Council
                Award ID: NE/J007064/1
                Funded by: The Human Science Frontier Programme
                Award ID: RGY0081/2012
                Funded by: Imperial College Junior Research Fellowship
                Categories
                Original Research
                Original Research
                Custom metadata
                2.0
                ece32818
                March 2017
                Converter:WILEY_ML3GV2_TO_NLMPMC version:5.0.8 mode:remove_FC converted:16.03.2017

                Evolutionary Biology
                bacteriophage,coevolution,evolution,parasitism,quorum sensing,resistance
                Evolutionary Biology
                bacteriophage, coevolution, evolution, parasitism, quorum sensing, resistance

                Comments

                Comment on this article