Bacteriophages and their genomes

Abstract

Bacteriophages occupy a unique position in biology, representing an absolute majority of all organisms in the biosphere. Because their genomes are relatively small, elucidating the genetic diversity of the phage population, deciphering their origins, and identifying the evolutionary mechanisms that shape the population would seem readily feasible. And yet the pace of phage genome characterization has slowed over the past three years, reflecting in part a need to transition from sequencing known and well-characterized bacteriophages to the isolation and comparative analysis of new isolates. The current state of bacteriophage genomics shows that the genetic diversity of the population is very high, that phages have been actively evolving for billions of years with active engagement of horizontal genetic exchange, and that their genomes are consequently pervasively mosaic in their architectures. But we have barely scratched the surface and the next years of phage genome exploration promise to be especially revealing.

Figure 1. Recent recombination events giving rise to phage genome mosaicism

Genetic exchange events giving rise to genome mosaicism are usually only observed at the nucleotide sequence level when the events have occurred relatively recently in evolutionary time. Mycobacteriophages Colbert, Rosebush and Qyrzula share similar overall genome architectures and many genes, but only Rosebush and Qyrzula have extensive nucleotide sequence similarity. A segment of Colbert containing genes 33–35 appears to have been acquired recently from a Rosebush-like phage, and the conserved sequences share 94% nucleotide identity. The extent of nucleotide similarity is displayed by coloring between the genomes, color-coded by spectrum with violet being the most similar and red the least. Predicted genes are shown as boxes, with gene numbers in the boxes and the sequence phamilies [24] above, with the number of phamily members shown in brackets; phamilies correspond to groups of related genes [24]. Genes are colored according to their phamily membership. Note that the apparent sites of recombination are located close to gene boundaries. The functions of most of these genes are not known but are predicted to be involved in tail assembly. Maps were generated using the program Phamerator (S. Cresawn, manuscript submitted).

Figure 2. Illustrations of phage genome mosaicism

A small segment of the mycobacteriophage Wildcat genome is shown encompassing genes 129–142. Genes are drawn and annotated as in Figure 1; those that have no homologues among the collection of mycobacteriophage genomes are shown as white boxes. The phylogenetic relationships of the three genes (134, 136 and 137) are represented as phamily circles, in which all genomes within the Phamerator database (S. Cresawn, manuscript submitted) are positioned around the circumference of the circle, and arcs are drawn between those phages sharing members of the phamily, with the thickness of the line reflecting the strength of sequence similarity. Each of the genes in Phams 236, 2040 and 990 clearly has a distinct evolutionary history.