Widespread genetic exchange among terrestrial bacteriophages

Abstract

Bacteriophages are the most numerous entities in the biosphere. Despite this numerical dominance, the genetic structure of bacteriophage populations is poorly understood. Here, we present a biogeography study involving 25 previously undescribed bacteriophages from the Cystoviridae clade, a group characterized by a dsRNA genome divided into three segments. Previous laboratory manipulation has shown that, when multiple Cystoviruses infect a single host cell, they undergo (i) rare intrasegment recombination events and (ii) frequent genetic reassortment between segments. Analyzing linkage disequilibrium (LD) within segments, we find no significant evidence of intrasegment recombination in wild populations, consistent with (i). An extensive analysis of LD between segments supports frequent reassortment, on a time scale similar to the genomic mutation rate. The absence of LD within this group of phages is consistent with expectations for a completely sexual population, despite the fact that some segments have >50% nucleotide divergence at 4-fold degenerate sites. This extraordinary rate of genetic exchange between highly unrelated individuals is unprecedented in any taxa. We discuss our results in light of the biological species concept applied to viruses.sex ͉ virus ͉ linkage disequilibrium ͉ Cystoviridae ͉ biogeography

New enveloped dsRNA phage from freshwater habitat

“…However, it has been shown that bacteriophages with a tripartite dsRNA genome can be readily isolated from agricultural plant species (Mindich et al, 1999;O'Keefe et al, 2010;Silander et al, 2005;Qiao et al, 2010). Although these additional viral isolates have not been specifically identified or classified, their high frequency in agricultural samples indicates that dsRNA bacteriophages are more common in terrestrial habitats than previously estimated.…”

“…The frequent genome segment reassortment of cystoviruses has been demonstrated in laboratory conditions and in nature (Onodera et al, 2001;Silander et al, 2005). Such a phenomenon could also explain the higher sequence variability between the M-segments of wNN and w6 compared with the other two segments.…”

“…Reassortment of genome segments occurs frequently among cystoviruses in laboratory conditions as well as in nature (Onodera et al, 2001;Silander et al, 2005). Surprisingly, the rate of reassortment may vary among populations sampled from different geographical locations (O'Keefe et al, 2010).…”

“…Exogenous genetic material, such as cellular transcripts or RNA strands from other viruses, may also be incorporated into cystovirus procapsids and recombine with endogenous viral RNA (Onodera et al, 2001). However, the probability of the packaging of two cystoviral RNA molecules of the same segment class into the same procapsid is very low owing to the strictly controlled packaging mechanism (Mindich, 1999), making homologous recombination an extremely rare event, both in vitro (Onodera et al, 2001) and in natural populations (Silander et al, 2005).…”

“…In addition to Pseudomonas phage w6 (Vidaver et al, 1973), the type virus of the Cystoviridae, several putative cystoviruses have been isolated (Mindich et al, 1999;O'Keefe et al, 2010;Silander et al, 2005;Qiao et al, 2010), but have not been formally classified by the International Committee on Taxonomy of Viruses. All isolates were obtained from plant debris in the USA, and they infect Gram-negative bacteria, mainly phytopathogenic Pseudomonas syringae strains.…”