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The population and evolutionary dynamics of homologous gene recombination in bacterial populations.

Levin BR, Cornejo OE - PLoS Genet. (2009)

Bottom Line: Using a semi-stochastic simulation of mutation, recombination, and selection within bacterial populations and competition between populations, we explore (1) the contribution of HGR to the rate of adaptive evolution in these populations and (2) the conditions under which HGR will provide a bacterial population a selective advantage over non-recombining or more slowly recombining populations.The results of our simulation indicate that, under broad conditions: (1) HGR occurring at rates in the range anticipated for bacteria like Streptococcus pneumoniae, Escherichia coli, Haemophilus influenzae, and Bacillus subtilis will accelerate the rate at which a population adapts to environmental conditions; (2) once established in a population, selection for this capacity to increase rates of adaptive evolution can maintain bacteria-encoded mechanisms of recombination and prevent invasion of non-recombining populations, even when recombination engenders a modest fitness cost; and (3) because of the density- and frequency-dependent nature of HGR in bacteria, this capacity to increase rates of adaptive evolution is not sufficient as a selective force to provide a recombining population a selective advantage when it is rare.Under realistic conditions, homologous gene recombination will increase the rate of adaptive evolution in bacterial populations and, once established, selection for higher rates of evolution will promote the maintenance of bacteria-encoded mechanisms for HGR.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Emory University, Atlanta, GA, USA. blevin@emory.edu

ABSTRACT
In bacteria, recombination is a rare event, not a part of the reproductive process. Nevertheless, recombination -- broadly defined to include the acquisition of genes from external sources, i.e., horizontal gene transfer (HGT) -- plays a central role as a source of variation for adaptive evolution in many species of bacteria. Much of niche expansion, resistance to antibiotics and other environmental stresses, virulence, and other characteristics that make bacteria interesting and problematic, is achieved through the expression of genes and genetic elements obtained from other populations of bacteria of the same and different species, as well as from eukaryotes and archaea. While recombination of homologous genes among members of the same species has played a central role in the development of the genetics and molecular biology of bacteria, the contribution of homologous gene recombination (HGR) to bacterial evolution is not at all clear. Also, not so clear are the selective pressures responsible for the evolution and maintenance of transformation, the only bacteria-encoded form of HGR. Using a semi-stochastic simulation of mutation, recombination, and selection within bacterial populations and competition between populations, we explore (1) the contribution of HGR to the rate of adaptive evolution in these populations and (2) the conditions under which HGR will provide a bacterial population a selective advantage over non-recombining or more slowly recombining populations. The results of our simulation indicate that, under broad conditions: (1) HGR occurring at rates in the range anticipated for bacteria like Streptococcus pneumoniae, Escherichia coli, Haemophilus influenzae, and Bacillus subtilis will accelerate the rate at which a population adapts to environmental conditions; (2) once established in a population, selection for this capacity to increase rates of adaptive evolution can maintain bacteria-encoded mechanisms of recombination and prevent invasion of non-recombining populations, even when recombination engenders a modest fitness cost; and (3) because of the density- and frequency-dependent nature of HGR in bacteria, this capacity to increase rates of adaptive evolution is not sufficient as a selective force to provide a recombining population a selective advantage when it is rare. Under realistic conditions, homologous gene recombination will increase the rate of adaptive evolution in bacterial populations and, once established, selection for higher rates of evolution will promote the maintenance of bacteria-encoded mechanisms for HGR. On the other hand, increasing rates of adaptive evolution by HGR is unlikely to be the sole or even a dominant selective pressure responsible for the original evolution of transformation.

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Time to reach the maximum mean fitness  for different rates of mutation and recombination.For the mutation rates (μ) −8 is 10−8, and −7 is 10−7 per cell per hour. For the recombination rate constants (χ), 0 is no recombination, −15 is χ = 10−15, −14 is χ = 10−14. In all simulations c = 0.5, e = 1 and density and total population size is 108 cells per ml. Means and standard errors of the time to reach maximum fitness for 50 runs with each set of parameters. (A) Runs initiated with a single intermediate fitness clone, 2,2,2,2,2. (B) Runs initiated with 10 randomly chosen clones.
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pgen-1000601-g005: Time to reach the maximum mean fitness for different rates of mutation and recombination.For the mutation rates (μ) −8 is 10−8, and −7 is 10−7 per cell per hour. For the recombination rate constants (χ), 0 is no recombination, −15 is χ = 10−15, −14 is χ = 10−14. In all simulations c = 0.5, e = 1 and density and total population size is 108 cells per ml. Means and standard errors of the time to reach maximum fitness for 50 runs with each set of parameters. (A) Runs initiated with a single intermediate fitness clone, 2,2,2,2,2. (B) Runs initiated with 10 randomly chosen clones.

Mentions: To provide an overview of the relative contributions of mutation and recombination to the rate of evolution in this model, we did fifty simulations with different mutation and recombination rates. We started these runs with either a single genotype of intermediate fitness, 2,2,2,2,2 genotype, or 10 randomly chosen clones (Figures 5A and 5B, respectively). In these figures we plot the mean and standard error of the time required for the mean fitness of the population to reach 0.001 less the maximum fitness, . As anticipated from the results presented in Figures 3 and 4, the time to reach maximum fitness decreases with the rates of recombination and mutation. Saying this another way the rate of adaptive evolution increases with the rate of recombination and mutation. Although the mutation process is biased towards generating lower fitness alleles, with only five loci and the fitness and other parameters employed, the effects of generating less fit mutations on the average fitness are imperceptible. This is the case even with a mutation rate of 10−5, all of the variation in fitness determined by these five loci, c = 0, and populations initiated with the highest fitness genotype 3,3,3,3,3 (data not shown). Although lower fitness mutants are produced, they are purged by “purifying” selection and do not accumulate.


The population and evolutionary dynamics of homologous gene recombination in bacterial populations.

Levin BR, Cornejo OE - PLoS Genet. (2009)

Time to reach the maximum mean fitness  for different rates of mutation and recombination.For the mutation rates (μ) −8 is 10−8, and −7 is 10−7 per cell per hour. For the recombination rate constants (χ), 0 is no recombination, −15 is χ = 10−15, −14 is χ = 10−14. In all simulations c = 0.5, e = 1 and density and total population size is 108 cells per ml. Means and standard errors of the time to reach maximum fitness for 50 runs with each set of parameters. (A) Runs initiated with a single intermediate fitness clone, 2,2,2,2,2. (B) Runs initiated with 10 randomly chosen clones.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2717328&req=5

pgen-1000601-g005: Time to reach the maximum mean fitness for different rates of mutation and recombination.For the mutation rates (μ) −8 is 10−8, and −7 is 10−7 per cell per hour. For the recombination rate constants (χ), 0 is no recombination, −15 is χ = 10−15, −14 is χ = 10−14. In all simulations c = 0.5, e = 1 and density and total population size is 108 cells per ml. Means and standard errors of the time to reach maximum fitness for 50 runs with each set of parameters. (A) Runs initiated with a single intermediate fitness clone, 2,2,2,2,2. (B) Runs initiated with 10 randomly chosen clones.
Mentions: To provide an overview of the relative contributions of mutation and recombination to the rate of evolution in this model, we did fifty simulations with different mutation and recombination rates. We started these runs with either a single genotype of intermediate fitness, 2,2,2,2,2 genotype, or 10 randomly chosen clones (Figures 5A and 5B, respectively). In these figures we plot the mean and standard error of the time required for the mean fitness of the population to reach 0.001 less the maximum fitness, . As anticipated from the results presented in Figures 3 and 4, the time to reach maximum fitness decreases with the rates of recombination and mutation. Saying this another way the rate of adaptive evolution increases with the rate of recombination and mutation. Although the mutation process is biased towards generating lower fitness alleles, with only five loci and the fitness and other parameters employed, the effects of generating less fit mutations on the average fitness are imperceptible. This is the case even with a mutation rate of 10−5, all of the variation in fitness determined by these five loci, c = 0, and populations initiated with the highest fitness genotype 3,3,3,3,3 (data not shown). Although lower fitness mutants are produced, they are purged by “purifying” selection and do not accumulate.

Bottom Line: Using a semi-stochastic simulation of mutation, recombination, and selection within bacterial populations and competition between populations, we explore (1) the contribution of HGR to the rate of adaptive evolution in these populations and (2) the conditions under which HGR will provide a bacterial population a selective advantage over non-recombining or more slowly recombining populations.The results of our simulation indicate that, under broad conditions: (1) HGR occurring at rates in the range anticipated for bacteria like Streptococcus pneumoniae, Escherichia coli, Haemophilus influenzae, and Bacillus subtilis will accelerate the rate at which a population adapts to environmental conditions; (2) once established in a population, selection for this capacity to increase rates of adaptive evolution can maintain bacteria-encoded mechanisms of recombination and prevent invasion of non-recombining populations, even when recombination engenders a modest fitness cost; and (3) because of the density- and frequency-dependent nature of HGR in bacteria, this capacity to increase rates of adaptive evolution is not sufficient as a selective force to provide a recombining population a selective advantage when it is rare.Under realistic conditions, homologous gene recombination will increase the rate of adaptive evolution in bacterial populations and, once established, selection for higher rates of evolution will promote the maintenance of bacteria-encoded mechanisms for HGR.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Emory University, Atlanta, GA, USA. blevin@emory.edu

ABSTRACT
In bacteria, recombination is a rare event, not a part of the reproductive process. Nevertheless, recombination -- broadly defined to include the acquisition of genes from external sources, i.e., horizontal gene transfer (HGT) -- plays a central role as a source of variation for adaptive evolution in many species of bacteria. Much of niche expansion, resistance to antibiotics and other environmental stresses, virulence, and other characteristics that make bacteria interesting and problematic, is achieved through the expression of genes and genetic elements obtained from other populations of bacteria of the same and different species, as well as from eukaryotes and archaea. While recombination of homologous genes among members of the same species has played a central role in the development of the genetics and molecular biology of bacteria, the contribution of homologous gene recombination (HGR) to bacterial evolution is not at all clear. Also, not so clear are the selective pressures responsible for the evolution and maintenance of transformation, the only bacteria-encoded form of HGR. Using a semi-stochastic simulation of mutation, recombination, and selection within bacterial populations and competition between populations, we explore (1) the contribution of HGR to the rate of adaptive evolution in these populations and (2) the conditions under which HGR will provide a bacterial population a selective advantage over non-recombining or more slowly recombining populations. The results of our simulation indicate that, under broad conditions: (1) HGR occurring at rates in the range anticipated for bacteria like Streptococcus pneumoniae, Escherichia coli, Haemophilus influenzae, and Bacillus subtilis will accelerate the rate at which a population adapts to environmental conditions; (2) once established in a population, selection for this capacity to increase rates of adaptive evolution can maintain bacteria-encoded mechanisms of recombination and prevent invasion of non-recombining populations, even when recombination engenders a modest fitness cost; and (3) because of the density- and frequency-dependent nature of HGR in bacteria, this capacity to increase rates of adaptive evolution is not sufficient as a selective force to provide a recombining population a selective advantage when it is rare. Under realistic conditions, homologous gene recombination will increase the rate of adaptive evolution in bacterial populations and, once established, selection for higher rates of evolution will promote the maintenance of bacteria-encoded mechanisms for HGR. On the other hand, increasing rates of adaptive evolution by HGR is unlikely to be the sole or even a dominant selective pressure responsible for the original evolution of transformation.

Show MeSH
Related in: MedlinePlus