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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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Five-locus, three allele simulation of mutation, recombination, selection and a bacterial population.
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pgen-1000601-g001: Five-locus, three allele simulation of mutation, recombination, selection and a bacterial population.

Mentions: In this simulation we consider a population of bacteria in mass (liquid) culture and five loci each with three alleles designated, 1, 2 and 3. P(I,J,K,L,M) is the relative frequency of the I,J,K,L,M genotype where, I, J, K, L and M take values 1, 2, or 3 and ∑I∑J∑K∑L∑M P(I,J,K,L,M) = 1; there are 35 = 243 possible genotypes. We assume that the fitness of a genotype is proportional to the sum of the values of the alleles to some power, e (e≥1), with all five genes contributing equally to fitness. We also assume that the contribution of the number 2 allele at any locus is intermediate between that of the number 1 and number 3 alleles. Thus the fitness of a genotype I,J,K,L,M,Where (1−c) is a measure of the extent to which these five loci contribute to fitness. For example with c = 0, and e = 1, the fitness of a genotype, 1,2,2,3,1 would be 9/10 = 0.90. The total range of fitness values would be 0.5 to 1.5, with 1,1,1,1,1 being the genotype of lowest fitness and 3,3,3,3,3 being the genotype of highest fitness. If c = 0.5 and e = 2, the range of fitness values would be 0.625 for the 1,1,1,1,1 genotype to 1.625 for the 3,3,3,3,3 genotype. With this fitness function, the 2,2,2,2,2 genotype would have a relative fitness of 1.0 independently of the value of e. The course of this simulation is diagrammed in Figure 1. In the following we describe the different steps in the simulation


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

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

Five-locus, three allele simulation of mutation, recombination, selection and a bacterial population.
© Copyright Policy
Related In: Results  -  Collection

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

pgen-1000601-g001: Five-locus, three allele simulation of mutation, recombination, selection and a bacterial population.
Mentions: In this simulation we consider a population of bacteria in mass (liquid) culture and five loci each with three alleles designated, 1, 2 and 3. P(I,J,K,L,M) is the relative frequency of the I,J,K,L,M genotype where, I, J, K, L and M take values 1, 2, or 3 and ∑I∑J∑K∑L∑M P(I,J,K,L,M) = 1; there are 35 = 243 possible genotypes. We assume that the fitness of a genotype is proportional to the sum of the values of the alleles to some power, e (e≥1), with all five genes contributing equally to fitness. We also assume that the contribution of the number 2 allele at any locus is intermediate between that of the number 1 and number 3 alleles. Thus the fitness of a genotype I,J,K,L,M,Where (1−c) is a measure of the extent to which these five loci contribute to fitness. For example with c = 0, and e = 1, the fitness of a genotype, 1,2,2,3,1 would be 9/10 = 0.90. The total range of fitness values would be 0.5 to 1.5, with 1,1,1,1,1 being the genotype of lowest fitness and 3,3,3,3,3 being the genotype of highest fitness. If c = 0.5 and e = 2, the range of fitness values would be 0.625 for the 1,1,1,1,1 genotype to 1.625 for the 3,3,3,3,3 genotype. With this fitness function, the 2,2,2,2,2 genotype would have a relative fitness of 1.0 independently of the value of e. The course of this simulation is diagrammed in Figure 1. In the following we describe the different steps in the simulation

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