Genomes of the T4-related bacteriophages as windows on microbial genome evolution

Abstract

The T4-related bacteriophages are a group of bacterial viruses that share morphological similarities and genetic homologies with the well-studied Escherichia coli phage T4, but that diverge from T4 and each other by a number of genetically determined characteristics including the bacterial hosts they infect, the sizes of their linear double-stranded (ds) DNA genomes and the predicted compositions of their proteomes. The genomes of about 40 of these phages have been sequenced and annotated over the last several years and are compared here in the context of the factors that have determined their diversity and the diversity of other microbial genomes in evolution. The genomes of the T4 relatives analyzed so far range in size between ~160,000 and ~250,000 base pairs (bp) and are mosaics of one another, consisting of clusters of homology between them that are interspersed with segments that vary considerably in genetic composition between the different phage lineages. Based on the known biological and biochemical properties of phage T4 and the proteins encoded by the T4 genome, the T4 relatives reviewed here are predicted to share a genetic core, or "Core Genome" that determines the structural design of their dsDNA chromosomes, their distinctive morphology and the process of their assembly into infectious agents (phage morphogenesis). The Core Genome appears to be the most ancient genetic component of this phage group and constitutes a mere 12-15% of the total protein encoding potential of the typical T4-related phage genome. The high degree of genetic heterogeneity that exists outside of this shared core suggests that horizontal DNA transfer involving many genetic sources has played a major role in diversification of the T4-related phages and their spread to a wide spectrum of bacterial species domains in evolution. We discuss some of the factors and pathways that might have shaped the evolution of these phages and point out several parallels between their diversity and the diversity generally observed within all groups of interrelated dsDNA microbial genomes in nature.

Figure 1

The protein products of the Core Genome of the T4-like Viruses. The functions of the phage gene products ("gp" designations) mentioned in this Figure are discussed in the text and summarized in Table 3.

Figure 2

Distribution of genome sizes among the sequenced T4 related phages (Table 2). The graphic highlights the distribution of phage genome sizes (red diamond shapes) in each of the bacterial host-specificity domains from which T4-related phages have been isolated (Table 1).

Figure 3

Divergence of the organization of Core genes among different types of T4-related genomes. The numbers and acronyms shown alongside the color-coded bars refer to the names of the phage-encoded genes and proteins listed in Table 3, which also summarizes their specific biochemical roles. DNA replication genes are color-coded dark blue, the recombination/repair genes light blue, the transcription and translation genes green, the morphogenetic genes red and the genes for aerobic nucleotide reductase (nrdAB) orange.