Dataset Information

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies.

ABSTRACT: Communication has been suggested as a mechanism to stabilize cooperation. In bacteria, chemical communication, termed quorum sensing (QS), has been hypothesized to fill this role, and extracellular public goods are often induced by QS at high cell densities. Here we show, with the bacterium Vibrio harveyi, that QS provides strong resistance against invasion of a QS defector strain by maximizing the cellular growth rate at low cell densities while achieving maximum productivity through protease upregulation at high cell densities. In contrast, QS mutants that act as defectors or unconditional cooperators maximize either the growth rate or the growth yield, respectively, and thus are less fit than the wild-type QS strain. Our findings provide experimental evidence that regulation mediated by microbial communication can optimize growth strategies and stabilize cooperative phenotypes by preventing defector invasion, even under well-mixed conditions. This effect is due to a combination of responsiveness to environmental conditions provided by QS, lowering of competitive costs when QS is not induced, and pleiotropic constraints imposed on defectors that do not perform QS.

Importance

Cooperation is a fundamental problem for evolutionary biology to explain. Conditional participation through phenotypic plasticity driven by communication is a potential solution to this dilemma. Thus, among bacteria, QS has been proposed to be a proximate stabilizing mechanism for cooperative behaviors. Here, we empirically demonstrate that QS in V. harveyi prevents cheating and subsequent invasion by nonproducing defectors by maximizing the growth rate at low cell densities and the growth yield at high cell densities, whereas an unconditional cooperator is rapidly driven to extinction by defectors. Our findings provide experimental evidence that QS regulation prevents the invasion of cooperative populations by QS defectors even under unstructured conditions, and they strongly support the role of communication in bacteria as a mechanism that stabilizes cooperative traits.

SUBMITTER: Bruger EL

PROVIDER: S-EPMC5086544 | biostudies-literature | 2016 Nov

REPOSITORIES: biostudies-literature

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Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies.

Bruger Eric L EL Waters Christopher M CM

Applied and environmental microbiology 20161027 22

Communication has been suggested as a mechanism to stabilize cooperation. In bacteria, chemical communication, termed quorum sensing (QS), has been hypothesized to fill this role, and extracellular public goods are often induced by QS at high cell densities. Here we show, with the bacterium Vibrio harveyi, that QS provides strong resistance against invasion of a QS defector strain by maximizing the cellular growth rate at low cell densities while achieving maximum productivity through protease u ...[more]

PMID: 27565619

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Project description:Quorum sensing (QS) is a form of bacterial chemical communication that regulates cellular phenotypes, including certain cooperative behaviors, in response to environmental and demographic changes. Despite the existence of proposed mechanisms that stabilize QS against defector exploitation, it is unclear if or how QS cooperators can proliferate in some model systems in populations mostly consisting of defectors. We predicted that growth in fragmented subpopulations could allow QS cooperators to invade a QS defector population. This could occur despite cooperators having lower relative fitnesses than defectors due to favored weighting of genotypes that produce larger populations of bacteria. Mixed metapopulations of Vibrio QS-proficient or unconditional cooperators and QS defectors were diluted and fragmented into isolated subpopulations in an environment that requires QS-regulated public good production to achieve larger population yields. Under these conditions, we observed global invasions of both cooperator genotypes into populations composed of primarily defectors. This spatially dependent increase in cooperator frequency was replicated for QS cooperators when mixed populations were competed in soft agar motility plates under conditions that allowed cooperators to disperse and outcompete defectors at the population edge, despite being less motile in isolation than defectors. These competition results show that the coordinated growth and dispersal of QS cooperators to additional resources is heavily favored in comparison to unconditional cooperation, and that dispersal of cooperators by motility into new environments, examined here in laboratory populations, constitutes a key mechanism for maintaining QS-regulated cooperation in the face of defection.IMPORTANCE Behaviors that are cooperative in nature are at risk of exploitation by cheating and are thus difficult to maintain by natural selection alone. While bacterial cell-cell communication, known as quorum sensing (QS), can stabilize microbial cooperative behaviors and is widespread in Vibrio species, it is unclear how QS can increase the frequency of cooperative strains in the presence of defectors without additional mechanisms. In this study, we demonstrate under multiple conditions that QS-mediated cooperation can increase in populations of Vibrio strains when cells experience narrow population bottlenecks or disperse from defectors. This occurred for both conditional cooperation mediated by QS and for unconditional cooperation, although conditional cooperators were better able to stabilize cooperation over a much wider range of conditions. Thus, we observed that population structuring allowed for assortment of competing genotypes and promoted cooperation via kin selection in microbes in a QS-dependent manner.

Project description:With the rising development of bacterial resistance the search for new medical treatments beyond conventional antimicrobials has become a key aim of public health research. Possible innovative strategies include the inhibition of bacterial virulence. However, consideration must be given to the evolutionary and environmental consequences of such new interventions. Virulence and cooperative social behaviour of the bacterium Pseudomonas aeruginosa rely on the quorum-sensing (QS) controlled production of extracellular products (public goods). Hence QS is an attractive target for anti-virulence interventions. During colonization, non-cooperating (and hence less virulent) P. aeruginosa QS-mutants, benefiting from public goods provided by wild type isolates, naturally increase in frequency providing a relative protection from invasive infection. We hypothesized that inhibition of QS-mediated gene expression removes this growth advantage and selection of less virulent QS-mutants, and maintains the predominance of more virulent QS-wild type bacteria. We addressed this possibility in a placebo-controlled trial investigating the anti-QS properties of azithromycin, a macrolide antibiotic devoid of bactericidal activity on P. aeruginosa, but interfering with QS, in intubated patients colonized by P. aeruginosa. In the absence of azithromycin, non-cooperating (and hence less virulent) lasR (QS)-mutants increased in frequency over time. Azithromycin significantly reduced QS-gene expression measured directly in tracheal aspirates. Concomitantly the advantage of lasR-mutants was lost and virulent wild-type isolates predominated during azithromycin treatment. We confirmed these results in vitro with fitness and invasion experiments. Azithromycin reduced growth rate of the wild-type, but not of the lasR-mutant. Furthermore, the lasR-mutant efficiently invaded wild-type populations in the absence, but not in the presence of azithromycin. These in vivo and in vitro results demonstrate that anti-virulence interventions based on QS-blockade diminish natural selection towards reduced virulence and therefore may increase the prevalence of more virulent genotypes in the Hospital environment. More generally, the impact of intervention on the evolution of virulence of pathogenic bacteria should be assessed.

Dataset Information

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies.

Importance

Publications

Bacterial Quorum Sensing Stabilizes Cooperation by Optimizing Growth Strategies.

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