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Intergenic incompatibilities reduce fitness in hybrids of extremely closely related bacteriophages.

ABSTRACT: Horizontal gene transfer and recombination occur across many groups of viruses and play key roles in important viral processes such as host-range expansion and immune-system avoidance. To have any predictive power regarding the ability of viruses to readily recombine, we must determine the extent to which epistasis restricts the success of recombinants, particularly as it relates to the genetic divergence between parental strains. In any hybridization event, the evolutionary success or failure of hybrids is largely determined by the pervasiveness of epistasis in the parental genomes. Recombination has previously been shown to incur steep fitness costs in highly divergent viruses as a result of disrupted epistatic interactions. We used a pair of bacteriophages of the family Microviridae to demonstrate that epistasis may evidence itself in the form of fitness costs even in the case of the exchange of alleles at a locus with amino acid divergence as low as 1%. We explored a possible biophysical source of epistasis in the interaction of viral coat and scaffolding proteins and examined a recovery mutation that likely repairs interactions disrupted by recombination.

SUBMITTER: Sackman AM

PROVIDER: S-EPMC4627924 | biostudies-literature | 2015

REPOSITORIES: biostudies-literature

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Intergenic incompatibilities reduce fitness in hybrids of extremely closely related bacteriophages.

Sackman Andrew M AM Reed Danielle D Rokyta Darin R DR

PeerJ 20151022

Horizontal gene transfer and recombination occur across many groups of viruses and play key roles in important viral processes such as host-range expansion and immune-system avoidance. To have any predictive power regarding the ability of viruses to readily recombine, we must determine the extent to which epistasis restricts the success of recombinants, particularly as it relates to the genetic divergence between parental strains. In any hybridization event, the evolutionary success or failure o ...[more]

PMID: 26528406

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Project description:Horizontal gene transfer and recombination play a major role in microbial evolution and have been detected in diverse groups, including many of medical relevance such as HIV and dengue virus. In the absence of mechanistic barriers, the evolutionary success of a particular recombination event is determined by whether the recombinant genotype suffers a fitness cost through the disruption of favorable epistatic interactions within the genome, and if so, the extent to which this fitness cost might be mitigated by subsequent compensatory evolution. To investigate the importance of epistatic interactions between genes and the evolutionary viability of a homologous recombination event between diverged ancestral genotypes, we constructed two recombinant microvirid bacteriophages by exchanging their alleles of the gene encoding the coat protein. The coding sequences for this gene differ by approximately 8% at the amino acid level and were interchanged between two ancestral phages related to varphiX174 and well adapted to their culture conditions. Because the recombinant phages showed drastically reduced fitnesses, we further explored their evolutionary viability by subjecting replicate lines of each of them to selection. We found that all four lineages achieved fitnesses commensurate with ancestral fitnesses in as few as 60 generations, and on average, the first substitution accounted for more than half of the total fitness recovery. Fitness recovery required three to five substitutions in each lineage, and overall eight of the nine essential phage genes were involved, suggesting extensive epistatic interactions throughout the genome. Interestingly, the proteins with the most extensive and apparent physical interactions with the exchanged protein in the viral capsid did not appear to have much of a role in fitness recovery. This result appears to be a consequence of the conservation of the amino acid residues involved in the interactions. It suggests that strong epistatic interactions are less important than weaker, transient ones in producing genic incompatibilities because they preclude variability in the interacting regions of the proteins.

Dataset Information

Intergenic incompatibilities reduce fitness in hybrids of extremely closely related bacteriophages.

Publications

Intergenic incompatibilities reduce fitness in hybrids of extremely closely related bacteriophages.

Similar Datasets

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