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Genetic information transfer promotes cooperation in bacteria.

ABSTRACT: Many bacterial species are social, producing costly secreted "public good" molecules that enhance the growth of neighboring cells. The genes coding for these cooperative traits are often propagated via mobile genetic elements and can be virulence factors from a biomedical perspective. Here, we present an experimental framework that links genetic information exchange and the selection of cooperative traits. Using simulations and experiments based on a synthetic bacterial system to control public good secretion and plasmid conjugation, we demonstrate that horizontal gene transfer can favor cooperation. In a well-mixed environment, horizontal transfer brings a direct infectious advantage to any gene, regardless of its cooperation properties. However, in a structured population transfer selects specifically for cooperation by increasing the assortment among cooperative alleles. Conjugation allows cooperative alleles to overcome rarity thresholds and invade bacterial populations structured purely by stochastic dilution effects. Our results provide an explanation for the prevalence of cooperative genes on mobile elements, and suggest a previously unidentified benefit of horizontal gene transfer for bacteria.

SUBMITTER: Dimitriu T

PROVIDER: S-EPMC4121819 | biostudies-literature | 2014 Jul

REPOSITORIES: biostudies-literature

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Genetic information transfer promotes cooperation in bacteria.

Dimitriu Tatiana T Lotton Chantal C Bénard-Capelle Julien J Misevic Dusan D Brown Sam P SP Lindner Ariel B AB Taddei François F

Proceedings of the National Academy of Sciences of the United States of America 20140714 30

Many bacterial species are social, producing costly secreted "public good" molecules that enhance the growth of neighboring cells. The genes coding for these cooperative traits are often propagated via mobile genetic elements and can be virulence factors from a biomedical perspective. Here, we present an experimental framework that links genetic information exchange and the selection of cooperative traits. Using simulations and experiments based on a synthetic bacterial system to control public ...[more]

PMID: 25024219

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Project description:When cooperation has a direct cost and an indirect benefit, a selfish behavior is more likely to be selected for than an altruistic one. Kin and group selection do provide evolutionary explanations for the stability of cooperation in nature, but we still lack the full understanding of the genomic mechanisms that can prevent cheater invasion. In our study we used Aevol, an agent-based, in silico genomic platform to evolve populations of digital organisms that compete, reproduce, and cooperate by secreting a public good for tens of thousands of generations. We found that cooperating individuals may share a phenotype, defined as the amount of public good produced, but have very different abilities to resist cheater invasion. To understand the underlying genetic differences between cooperator types, we performed bio-inspired genomics analyses of our digital organisms by recording and comparing the locations of metabolic and secretion genes, as well as the relevant promoters and terminators. Association between metabolic and secretion genes (promoter sharing, overlap via frame shift or sense-antisense encoding) was characteristic for populations with robust cooperation and was more likely to evolve when secretion was costly. In mutational analysis experiments, we demonstrated the potential evolutionary consequences of the genetic association by performing a large number of mutations and measuring their phenotypic and fitness effects. The non-cooperating mutants arising from the individuals with genetic association were more likely to have metabolic deleterious mutations that eventually lead to selection eliminating such mutants from the population due to the accompanying fitness decrease. Effectively, cooperation evolved to be protected and robust to mutations through entangled genetic architecture. Our results confirm the importance of second-order selection on evolutionary outcomes, uncover an important genetic mechanism for the evolution and maintenance of cooperation, and suggest promising methods for preventing gene loss in synthetically engineered organisms.

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.

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Genetic information transfer promotes cooperation in bacteria.

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Genetic information transfer promotes cooperation in bacteria.

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