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In silico bacteria evolve robust cooperaion via complex quorum-sensing strategies.

ABSTRACT: Many species of bacteria collectively sense and respond to their social and physical environment via 'quorum sensing' (QS), a communication system controlling extracellular cooperative traits. Despite detailed understanding of the mechanisms of signal production and response, there remains considerable debate over the functional role(s) of QS: in short, what is it for? Experimental studies have found support for diverse functional roles: density sensing, mass-transfer sensing, genotype sensing, etc. While consistent with theory, these results cannot separate whether these functions were drivers of QS adaption, or simply artifacts or 'spandrels' of systems shaped by distinct ecological pressures. The challenge of separating spandrels from drivers of adaptation is particularly hard to address using extant bacterial species with poorly understood current ecologies (let alone their ecological histories). To understand the relationship between defined ecological challenges and trajectories of QS evolution, we used an agent-based simulation modeling approach. Given genetic mixing, our simulations produce behaviors that recapitulate features of diverse microbial QS systems, including coercive (high signal/low response) and generalized reciprocity (signal auto-regulation) strategists - that separately and in combination contribute to QS-dependent resilience of QS-controlled cooperation in the face of diverse cheats. We contrast our in silico results given defined ecological challenges with bacterial QS architectures that have evolved under largely unknown ecological contexts, highlighting the critical role of genetic constraints in shaping the shorter term (experimental evolution) dynamics of QS. More broadly, we see experimental evolution of digital organisms as a complementary tool in the search to understand the emergence of complex QS architectures and functions.

SUBMITTER: Wang Y

PROVIDER: S-EPMC7248119 | biostudies-literature | 2020 May

REPOSITORIES: biostudies-literature

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In silico bacteria evolve robust cooperaion via complex quorum-sensing strategies.

Wang Yifei Y Rattray Jennifer B JB Thomas Stephen A SA Gurney James J Brown Sam P SP

Scientific reports 20200525 1

Many species of bacteria collectively sense and respond to their social and physical environment via 'quorum sensing' (QS), a communication system controlling extracellular cooperative traits. Despite detailed understanding of the mechanisms of signal production and response, there remains considerable debate over the functional role(s) of QS: in short, what is it for? Experimental studies have found support for diverse functional roles: density sensing, mass-transfer sensing, genotype sensing, ...[more]

PMID: 32451396

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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: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.ImportanceCooperation 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.

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In silico bacteria evolve robust cooperaion via complex quorum-sensing strategies.

Publications

In silico bacteria evolve robust cooperaion via complex quorum-sensing strategies.

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