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Within-host competition determines reproductive success of temperate bacteriophages.

ABSTRACT: Within-host competition between parasites is frequently invoked as a major force for parasite evolution, yet quantitative studies on its extent in an organismal group are lacking. Temperate bacteriophages are diverse and abundant parasites of bacteria, distinguished by their ability to enter a facultative dormant state in their host. Bacteria can accumulate multiple phages that may eventually abandon dormancy in response to host stress. Host resources are then converted into phage particles, whose release requires cell death. To study within-host competition between phages, I used the bacterium Escherichia coli and 11 lambdoid phages to construct single and double lysogens. Lysogenic bacterial cultures were then induced and time to host cell lysis and productivity of phages was measured. In double lysogens, this revealed strong competitive interactions as in all cases productivity of at least one phage declined. The outcome of within-host competition was often asymmetrical, and phages were found to vary hierarchically in within-host competitive ability. In double infections, the phage with the shorter lysis time determined the timing of cell lysis, which was associated with a competitive advantage when time differences were large. The results emphasize that within-host competition greatly affects phage fitness and that multiple infections should be considered an integral part of bacteriophage ecology.

SUBMITTER: Refardt D

PROVIDER: S-EPMC3160688 | biostudies-literature | 2011 Sep

REPOSITORIES: biostudies-literature

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Within-host competition determines reproductive success of temperate bacteriophages.

Refardt Dominik D

The ISME journal 20110317 9

Within-host competition between parasites is frequently invoked as a major force for parasite evolution, yet quantitative studies on its extent in an organismal group are lacking. Temperate bacteriophages are diverse and abundant parasites of bacteria, distinguished by their ability to enter a facultative dormant state in their host. Bacteria can accumulate multiple phages that may eventually abandon dormancy in response to host stress. Host resources are then converted into phage particles, who ...[more]

PMID: 21412345

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Project description:Within-host competition can affect outcomes of infections when parasites occupy the same niche. We investigated within-host competition and infection outcomes in Chinook salmon exposed to two genotypes of Ceratonova shasta (myxozoan parasite). We assessed i) virulence (host mortality, median days to death), ii) within-host competition (abundance in host), and iii) success (spore production, proportion of myxospore-producing hosts) following concurrent and sequential exposures to single or mixed-genotype treatments. In single treatments, genotype-I replicated faster, and caused higher and earlier host mortality (higher virulence) but genotype-II produced more myxospores (higher success). In mixed treatments, costs of competition were observed for both genotypes evidenced by reduced replication or myxospore production following concurrent exposures, but only the less-virulent genotype suffered costs of competition when hosts were exposed to genotypes sequentially. To understand potential host effects on competition outcomes, we characterized systemic (spleen) and local (intestine) cytokine and immunoglobulin expression in single and mixed infections. We observed delayed systemic and immunosuppressive responses to the virulent genotype (I), rapid, localized and non-suppressive responses to the less-virulent genotype (II), and a combination of responses to mixed-genotypes. Thus, competition outcomes favoring the virulent genotype may be partially explained by the localized response to genotype-II that facilitates myxospore production (success) offsetting the systemic response to genotype-I that results in early inflammation and immunosuppression (that increases onset of mortality). This evidence for different but simultaneous responses to each genotype suggests selection should favor the exclusion of the weaker competitor and the evolution of increased virulence in the stronger competitor because the outcome was generally more costly for the less-virulent genotype. With caveats, our results are relevant for understanding infection outcomes in commercially and ecologically important salmonids in C. shasta endemic regions where mixed infections are commonplace.

Project description:Variance in reproductive success (sk2, with k = number of offspring) plays a large role in determining the rate of genetic drift and the scope within which selection acts. Various frameworks have been proposed to parse factors that contribute to sk2, but none has focused on age-specific values of ϕ=sk2/k¯, which indicate the degree to which reproductive skew is overdispersed (compared to the random Poisson expectation) among individuals of the same age and sex. Instead, within-age effects are generally lumped with residual variance and treated as "noise." Here, an ANOVA sums-of-squares framework is used to partition variance in annual and lifetime reproductive success into between-group and within-group components. For annual reproduction, the between-age effect depends on age-specific fecundity (b x), but relatively few empirical data are available on the within-age effect, which depends on ϕ x. By defining groups by age-at-death rather than age, the same ANOVA framework can be used to partition variance in lifetime reproductive success (LRS) into between-group and within-group components. Analytical methods are used to develop null-model expectations for random contributions to within-group and between-group components. For analysis of LRS, random variation in longevity appears as part of the between-group variance, and effects (if any) of skip breeding and persistent individual differences contribute to the within-group variance. Simulations are used to show that the methods for variance partitioning are asymptotically unbiased. Practical application is illustrated with empirical data for annual reproduction in American black bears and lifetime reproduction in Dutch great tits. Results show that overdispersed within-age variance (1) dominates annual sk2 in both male and female black bears, (2) is the primary factor that reduces annual effective size to a fraction of the number of adults, and (3) represents most of the opportunity for selection. In contrast, about a quarter of the variance in LRS in great tits can be attributed to random variation in longevity, and most of the rest is due to modest differences in fecundity with age estimated for a single cohort of females. R code is provided that reads generic input files for annual and lifetime reproductive success and allows users to conduct variance partitioning with their own data.

Project description:BackgroundProphages integrated within the chromosomes of Campylobacter jejuni isolates have been demonstrated very recently. Prior work with Campylobacter temperate bacteriophages, as well as evidence from prophages in other enteric bacteria, suggests these prophages might have a role in the biology and virulence of the organism. However, very little is known about the genetic variability of Campylobacter prophages which, if present, could lead to differential phenotypes in isolates carrying the phages versus those that do not. As a first step in the characterization of C. jejuni prophages, we investigated the distribution of prophage DNA within a C. jejuni population assessed the DNA and protein sequence variability within a subset of the putative prophages found.ResultsSouthern blotting of C. jejuni DNA using probes from genes within the three putative prophages of the C. jejuni sequenced strain RM 1221 demonstrated the presence of at least one prophage gene in a large proportion (27/35) of isolates tested. Of these, 15 were positive for 5 or more of the 7 Campylobacter Mu-like phage 1 (CMLP 1, also designated Campylobacter jejuni integrated element 1, or CJIE 1) genes tested. Twelve of these putative prophages were chosen for further analysis. DNA sequencing of a 9,000 to 11,000 nucleotide region of each prophage demonstrated a close homology with CMLP 1 in both gene order and nucleotide sequence. Structural and sequence variability, including short insertions, deletions, and allele replacements, were found within the prophage genomes, some of which would alter the protein products of the ORFs involved. No insertions of novel genes were detected within the sequenced regions. The 12 prophages and RM 1221 had a % G+C very similar to C. jejuni sequenced strains, as well as promoter regions characteristic of C. jejuni. None of the putative prophages were successfully induced and propagated, so it is not known if they were functional or if they represented remnant prophage DNA in the bacterial chromosomes.ConclusionThese putative prophages form a family of phages with conserved sequences, and appear to be adapted to Campylobacter. There was evidence for recombination among groups of prophages, suggesting that the prophages had a mosaic structure. In many of these properties, the Mu-like CMLP 1 homologs characterized in this study resemble temperate bacteriophages of enteric bacteria that are responsible for contributions to virulence and host adaptation.

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Within-host competition determines reproductive success of temperate bacteriophages.

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Within-host competition determines reproductive success of temperate bacteriophages.

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