Horizontal Gene Transfer and the Evolution of Microvirid Coliphage Genomes

Abstract

Bacteriophage genomic evolution has been largely characterized by rampant, promiscuous horizontal gene transfer involving both homologous and nonhomologous source DNA. This pattern has emerged through study of the tailed double-stranded DNA (dsDNA) phages and is based upon a sparse sampling of the enormous diversity of these phages. The single-stranded DNA phages of the family Microviridae, including X174, appear to evolve through qualitatively different mechanisms, possibly as result of their strictly lytic lifestyle and small genome size. However, this apparent difference could reflect merely a dearth of relevant data. We sought to characterize the forces that contributed to the molecular evolution of the Microviridae and to examine the genetic structure of this single family of bacteriophage by sequencing the genomes of microvirid phage isolated on a single bacterial host. Microvirids comprised 3.5% of the detectable phage in our environmental samples, and sequencing yielded 42 new microvirid genomes. Phylogenetic analysis of the genes contained in these and five previously described microvirid phages identified three distinct clades and revealed at least two horizontal transfer events between clades. All members of one clade have a block of five putative genes that are not present in any member of the other two clades. Our data indicate that horizontal transfer does contribute to the evolution of the microvirids but is both quantitatively and qualitatively different from what has been observed for the dsDNA phages.

Environment Determines Epistatic Patterns for a ssDNA Virus

“…For the ssDNA phage fX174, which is a close relative of our wild-type phage ID11 (Rokyta et al 2006b), Vale et al (2012) found that, for 36 random mutations, fitness effects …”

“…In the present work, we attempted to shift the wild-type genotype, ID11, and its nine previously described beneficial mutations (Rokyta et al 2005(Rokyta et al , 2008(Rokyta et al , 2011 closer to and farther from the optimal phenotype by changing the temperature at which fitness was measured, to quantify the changes in fitness effects and patterns of epistatic interactions between mutations. Previous work has shown that close relatives of ID11 in the G4-like group of microvirid coliphages (Rokyta et al 2006b) tend to have fitnesses inversely correlated with temperature (Knies et al 2009). The original mutations were isolated by means of selection at 37°, and we therefore attempted to move the genotypes closer to the optimum by measuring fitnesses at a lower temperature (33°) and farther from the optimum by measuring fitnesses at a higher temperature (41°), leaving the genotypes involved constant.…”

Diversity and distribution of single-stranded DNA phages in the North Atlantic Ocean

“…Members of the Microviridae infecting a diverse range of hosts (including proteobacteria, Spiroplasma, Chlamydia) have been isolated and completely sequenced (Sanger et al, 1977;Renaudin et al, 1987;Storey et al, 1989;Lui et al, 2000;Read et al, 2000;Brentlinger et al, 2002;Garner et al, 2004;Rokyta et al, 2006). Genome comparisons have identified two distinct groups of Microviridae (those similar to the chlamydiaphages and those similar to Escherichia coli fX174), leading to the suggestion that ssDNA phages evolve through different mechanisms than dsDNA phages (Brentlinger et al, 2002;Rokyta et al, 2006). Although the Microviridae have been extensively studied, the sequenced representatives infect a small number of bacterial hosts.…”

Mutational Effects and Population Dynamics During Viral Adaptation Challenge Current Models

“…Research was conducted using the bacteriophage ID11, a member of family Microviridae described by Rokyta et al (2006b). ID11 is a single-stranded DNA icosahedral virus with a genome 5577 bases long encoding 11 genes.…”