The evolution of bacterial mutation rates under simultaneous selection by interspecific and social parasitism

O’Brien, Siobhán; Rodrigues, António M. M.; Buckling, Angus

doi:10.1098/rspb.2013.1913

Cited by 19 publications

(16 citation statements)

References 49 publications

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“…We note that hitchhiking effects may be disrupted by recombination (Barton, 2000), and that mutator advantage under parasitism also depends on ecological factors such as the structure of the abiotic environment (Gómez and Buckling, 2013). Nevertheless, our finding that an elevated mutation rate is advantageous under phage selection is also consistent with evidence that Pseudomonas fluorescens mutators are favoured during coevolution with phage F2 (Pál et al, 2007;O'Brien et al, 2013). The cost of antibiotic resistance as inferred by classical in vitro methods can also influence the likelihood of fixing under phage selection.…”

Section: Discussionsupporting

confidence: 79%

Lytic phages obscure the cost of antibiotic resistance in Escherichia coli

Tazzyman

Hall

2014

The ISME Journal

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The long-term persistence of antibiotic-resistant bacteria depends on their fitness relative to other genotypes in the absence of drugs. Outside the laboratory, viruses that parasitize bacteria (phages) are ubiquitous, but costs of antibiotic resistance are typically studied in phage-free experimental conditions. We used a mathematical model and experiments with Escherichia coli to show that lytic phages strongly affect the incidence of antibiotic resistance in drug-free conditions. Under phage parasitism, the likelihood that antibiotic-resistant genetic backgrounds spread depends on their initial frequency, mutation rate and intrinsic growth rate relative to drug-susceptible genotypes, because these parameters determine relative rates of phage-resistance evolution on different genetic backgrounds. Moreover, the average cost of antibiotic resistance in terms of intrinsic growth in the antibiotic-free experimental environment was small relative to the benefits of an increased mutation rate in the presence of phages. This is consistent with our theoretical work indicating that, under phage selection, typical costs of antibiotic resistance can be outweighed by realistic increases in mutability if drug resistance and hypermutability are genetically linked, as is frequently observed in clinical isolates. This suggests the long-term distribution of antibiotic resistance depends on the relative rates at which different lineages adapt to other types of selection, which in the case of phage parasitism is probably extremely common, as well as costs of resistance inferred by classical in vitro methods.

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Section: Discussionsupporting

confidence: 79%

Lytic phages obscure the cost of antibiotic resistance in Escherichia coli

Tazzyman

Hall

2014

The ISME Journal

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“…Bacterial infection by viruses (phages) is the most common host–parasite interaction on Earth, globally estimated at 10 25 infections per second (Pedulla et al 2003 ), and diverse phage-resistance mechanisms have been characterized (Labrie et al 2010 ). Phage selection can also cause alleles that modify bacterial mutation rates to spread through genetic hitchhiking, because resistance mutations are produced more frequently in mutator lineages (Pál et al 2007 ; Morgan et al 2010 ; O’Brien et al 2013 ). Both resistance and mutator alleles have important effects on bacterial evolutionary trajectories (Wielgoss et al 2013 ; Scanlan et al 2015 ), medical outcomes by altering bacterial growth rate and virulence (Smith and Huggins 1982 ; Capparelli et al 2010 ), and antibiotic resistance (Oliver et al 2000 ; Denamur et al 2002 ).…”

Section: Introductionmentioning

confidence: 99%

Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria

et al. 2015

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Parasitism creates selection for resistance mechanisms in host populations and is hypothesized to promote increased host evolvability. However, the influence of these traits on host evolution when parasites are no longer present is unclear. We used experimental evolution and whole-genome sequencing of Escherichia coli to determine the effects of past and present exposure to parasitic viruses (phages) on the spread of mutator alleles, resistance, and bacterial competitive fitness. We found that mutator alleles spread rapidly during adaptation to any of four different phage species, and this pattern was even more pronounced with multiple phages present simultaneously. However, hypermutability did not detectably accelerate adaptation in the absence of phages and recovery of fitness costs associated with resistance. Several lineages evolved phage resistance through elevated mucoidy, and during subsequent evolution in phage-free conditions they rapidly reverted to nonmucoid, phage-susceptible phenotypes. Genome sequencing revealed that this phenotypic reversion was achieved by additional genetic changes rather than by genotypic reversion of the initial resistance mutations. Insertion sequence (IS) elements played a key role in both the acquisition of resistance and adaptation in the absence of parasites; unlike single nucleotide polymorphisms, IS insertions were not more frequent in mutator lineages. Our results provide a genetic explanation for rapid reversion of mucoidy, a phenotype observed in other bacterial species including human pathogens. Moreover, this demonstrates that the types of genetic change underlying adaptation to fitness costs, and consequently the impact of evolvability mechanisms such as increased point-mutation rates, depend critically on the mechanism of resistance.

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“…Not only is phage predation a major driver of bacterial diversification (1,2), but it may also select for hypermutators, which could increase the frequency of mutations in bacterial populations (3,4). Whereas bacteria are limited to one cell division per generation, a single phage-infected cell can produce a burst ranging from less than 5 to over 1,000 progeny phages in a similar period of time (5)(6)(7).…”

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confidence: 99%

Selection and Characterization of Phage-Resistant Mutant Strains of Listeria monocytogenes Reveal Host Genes Linked to Phage Adsorption

Denes

Bakker

Tokman

et al. 2015

Appl Environ Microbiol

104

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Listeria-infecting phages are readily isolated from Listeria-containing environments, yet little is known about the selective forces they exert on their host. Here, we identified that two virulent phages, LP-048 and LP-125, adsorb to the surface of Listeria monocytogenes strain 10403S through different mechanisms. We isolated and sequenced, using whole-genome sequencing, 69 spontaneous mutant strains of 10403S that were resistant to either one or both phages. Mutations from 56 phage-resistant mutant strains with only a single mutation mapped to 10 genes representing five loci on the 10403S chromosome. An additional 12 mutant strains showed two mutations, and one mutant strain showed three mutations. Two of the loci, containing seven of the genes, accumulated the majority (n ‫؍‬ 64) of the mutations. A representative mutant strain for each of the 10 genes was shown to resist phage infection through mechanisms of adsorption inhibition. Complementation of mutant strains with the associated wild-type allele was able to rescue phage susceptibility for 6 out of the 10 representative mutant strains. Wheat germ agglutinin, which specifically binds to N-acetylglucosamine, bound to 10403S and mutant strains resistant to LP-048 but did not bind to mutant strains resistant to only LP-125. We conclude that mutant strains resistant to only LP-125 lack terminal N-acetylglucosamine in their wall teichoic acid (WTA), whereas mutant strains resistant to both phages have disruptive mutations in their rhamnose biosynthesis operon but still possess N-acetylglucosamine in their WTA. V irulent phages have been shown to present a tremendous selective pressure on their bacterial host populations. Not only is phage predation a major driver of bacterial diversification (1, 2), but it may also select for hypermutators, which could increase the frequency of mutations in bacterial populations (3, 4). Whereas bacteria are limited to one cell division per generation, a single phage-infected cell can produce a burst ranging from less than 5 to over 1,000 progeny phages in a similar period of time (5-7). Phages consequently have the capability to rapidly outgrow their bacterial hosts and can significantly reduce or eliminate susceptible bacteria in the local environment (8, 9). Therefore, the potential for bacterial strains to persist in an environment containing lytic phages may be contingent upon that strain accumulating spontaneous mutations that grant resistance to phage infection (10). These phage-resistant mutant strains most typically resist phage infection through mechanisms of adsorption inhibition, i.e., alterations of the cell surface that affect phage attachment (11). However, one study reported that nearly all phage-resistant mutant strains of Streptococcus thermophilus had acquired CRISPR spacers that matched invading phage genomes (12); these S. thermophilus mutant strains would be expected to resist phage infection after the adsorption step. Phage-resistant mutant strains that resist infection through mechanisms of adsorption inh...

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The evolution of bacterial mutation rates under simultaneous selection by interspecific and social parasitism

Cited by 19 publications

References 49 publications

Lytic phages obscure the cost of antibiotic resistance in Escherichia coli

Lytic phages obscure the cost of antibiotic resistance in Escherichia coli

Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria

Selection and Characterization of Phage-Resistant Mutant Strains of Listeria monocytogenes Reveal Host Genes Linked to Phage Adsorption

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