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Coevolutionary arms races between bacteria and bacteriophage.

ABSTRACT: We propose a computational and theoretical framework for analyzing rapid coevolutionary dynamics of bacteriophage and bacteria in their ecological context. Bacteriophage enter host cells via membrane-bound surface receptors often responsible for nutrient uptake. As such, a selective pressure will exist for the bacteria to modify its receptor configuration and, in turn, for the phage to modify its tail fiber. A mathematical model of these trait adaptations is developed by using the framework of adaptive dynamics. Host strains differ in their efficiency of resource uptake and resistance to phage, whereas phage strains differ in their host preference for adsorption. We solve the evolutionary ecology model and find the conditions for coevolutionary branching and relevant dimensionless parameters leading to distinct quasispecies. We confirm these calculations using stochastic Monte Carlo simulations of populations evolving in a chemostat with fixed washout rate and inflow resource density. We find that multiple quasispecies of bacteria and phage can coexist in a homogeneous medium with a single resource. When diversification occurs, quasispecies of phage adsorb effectively to only a limited subset of the total number of quasispecies of bacteria, i.e., functional differences between quasispecies arise endogenously within the evolutionary ecology framework. Finally, we discuss means to relate predictions of this model to experimental studies in the chemostat, using the model organisms Escherichia coli and the virulent strain of lambda phage.

SUBMITTER: Weitz JS

PROVIDER: S-EPMC1172273 | biostudies-literature | 2005 Jul

REPOSITORIES: biostudies-literature

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Coevolutionary arms races between bacteria and bacteriophage.

Weitz J S JS Hartman H H Levin S A SA

Proceedings of the National Academy of Sciences of the United States of America 20050623 27

We propose a computational and theoretical framework for analyzing rapid coevolutionary dynamics of bacteriophage and bacteria in their ecological context. Bacteriophage enter host cells via membrane-bound surface receptors often responsible for nutrient uptake. As such, a selective pressure will exist for the bacteria to modify its receptor configuration and, in turn, for the phage to modify its tail fiber. A mathematical model of these trait adaptations is developed by using the framework of a ...[more]

PMID: 15976021

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Project description:Viral receptors are the cell surface proteins that are hijacked by viruses to initialize their infections. Viral receptors are subject to two conflicting directional forces, namely, negative selection due to functional constraints and positive selection due to host-virus arms races. It remains largely obscure whether negative pleiotropy limits the rate of adaptation in viral receptors. Here, we perform evolutionary analyses of 96 viral receptor genes in primates and find that 41 out of 96 viral receptors experienced adaptive evolution. Many positively selected residues in viral receptors are located at the virus-receptor interfaces. Compared with control proteins, viral receptors exhibit significantly elevated rate of adaptation. Further analyses of genetic polymorphisms in human populations reveal signals of positive selection and balancing selection for 53 and 5 viral receptors, respectively. Moreover, we find that 49 viral receptors experienced different selection pressures in different human populations, indicating that viruses represent an important driver of local adaptation in humans. Our findings suggest that diverse viruses, many of which have not been known to infect nonhuman primates, have maintained antagonistic associations with primates for millions of years, and the host-virus conflicts drive accelerated adaptive evolution in viral receptors.IMPORTANCE Viruses hijack cellular proteins, termed viral receptors, to assist their entry into host cells. While viral receptors experience negative selection to maintain their normal functions, they also undergo positive selection due to an everlasting evolutionary arms race between viruses and hosts. A complete picture on how viral receptors evolve under two conflicting forces is still lacking. In this study, we systematically analyzed the evolution of 96 viral receptors in primates and human populations. We found around half of viral receptors underwent adaptive evolution and exhibit significantly elevated rates of adaptation compared to control genes in primates. We also found signals of past natural selection for 58 viral receptors in human populations. Interestingly, 49 viral receptors experienced different selection pressures in different human populations, indicating that viruses represent an important driver of local adaptation in humans. Our results suggest that host-virus arms races drive accelerated adaptive evolution in viral receptors.

Dataset Information

Coevolutionary arms races between bacteria and bacteriophage.

Publications

Coevolutionary arms races between bacteria and bacteriophage.

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