Abstract
Bacteriophages are the most prevalent biological entities impacting on the ecosystem and are characterized by their extensive diversity. However, there are two aspects of phages that have remained largely unexplored: genetic flux by recombination between phage populations and characterization of specific phages in terms of the pan-genome. Here, we examined the recombination and pan-genome in Helicobacter pylori prophages at both the genome and gene level. In the genome-level analysis, we applied, for the first time, chromosome painting and fineSTRUCTURE algorithms to a phage species, and showed novel trends in inter-population genetic flux. Notably, hpEastAsia is a phage population that imported a higher proportion of DNA fragments from other phages, whereas the hpSWEurope phages showed weaker signatures of inter-population recombination, suggesting genetic isolation. The gene-level analysis showed that, after parameter tuning of the prokaryote pan-genome analysis program, H. pylori phages have a pan-genome consisting of 75 genes and a soft-core genome of 10 genes, which includes genes involved in the lytic and lysogenic life cycles. Quantitative analysis of recombination events of the soft-core genes showed no substantial variation in the intensity of recombination across the genes, but rather equally frequent recombination among housekeeping genes that were previously reported to be less prone to recombination. The signature of frequent recombination appears to reflect the host–phage evolutionary arms race, either by contributing to escape from bacterial immunity or by protecting the host by producing defective phages.
Highlights
Viruses are the most prevalent biological entities on Earth; they play important roles in ecological balance and are characterized by their extensive diversity [8]
For 27 H. pylori prophages, 19 of which were predicted to be active using Phage Hunter [27] (Table S1), each complete genome was reconstructed using fragments (‘chunks’) of DNA donated by other individual genomes using the chromosome painting algorithm, as summarized and visualized in the co-ancestry matrix (Fig. 2)
The two-step approach is applicable even when the sample size is small, as shown previously in H. pylori, which is in contrast to STRUCTURE, which is based on allele frequency and requires at least 15–20 individuals per hypothesized population [20]
Summary
Viruses are the most prevalent biological entities on Earth; they play important roles in ecological balance and are characterized by their extensive diversity [8]. The high genetic diversity in phages is likely due to their ancient origin (they originated about 3 billion years ago), the huge number of phages present in the biosphere and their frequent infection of permissive hosts. These lead phages to encounter DNA derived from bacteria or prophages (phages integrated into bacterial chromosomes) with which they can recombine [10]. As a consequence of such recombination, most recombinants are defective for growth, and natural selection eliminates all but a very small
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