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. 2012;7(7):e40102.
doi: 10.1371/journal.pone.0040102. Epub 2012 Jul 6.

Phage morphology recapitulates phylogeny: the comparative genomics of a new group of myoviruses

André M Comeau  1 , Denise Tremblay, Sylvain Moineau, Thomas Rattei, Alla I Kushkina, Fedor I Tovkach, Henry M Krisch, Hans-Wolfgang Ackermann
Affiliations

Phage morphology recapitulates phylogeny: the comparative genomics of a new group of myoviruses

André M Comeau et al. PLoS One. 2012.

Abstract

Among dsDNA tailed bacteriophages (Caudovirales), members of the Myoviridae family have the most sophisticated virion design that includes a complex contractile tail structure. The Myoviridae generally have larger genomes than the other phage families. Relatively few "dwarf" myoviruses, those with a genome size of less than 50 kb such as those of the Mu group, have been analyzed in extenso. Here we report on the genome sequencing and morphological characterization of a new group of such phages that infect a diverse range of Proteobacteria, namely Aeromonas salmonicida phage 56, Vibrio cholerae phages 138 and CP-T1, Bdellovibrio phage φ1422, and Pectobacterium carotovorum phage ZF40. This group of dwarf myoviruses shares an identical virion morphology, characterized by usually short contractile tails, and have genome sizes of approximately 45 kb. Although their genome sequences are variable in their lysogeny, replication, and host adaption modules, presumably reflecting differing lifestyles and hosts, their structural and morphogenesis modules have been evolutionarily constrained by their virion morphology. Comparative genomic analysis reveals that these phages, along with related prophage genomes, form a new coherent group within the Myoviridae. The results presented in this communication support the hypothesis that the diversity of phages may be more structured than generally believed and that the innumerable phages in the biosphere all belong to discrete lineages or families.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. EM micrographs showing the morphology typical of the φPLPE group phages.
Presented are Aeromonas phage 56 (top, uranyl acetate), Bdellovibrio phage φ1422 (bottom left, phosphotungstate) and Vibrio phage 138 (bottom right, phosphotungstate). The scale bar is 100 nm and applies to all micrographs.
Figure 2
Figure 2. Comparative genomics of the eight φPLPE group phages.
Note that the previously published sequences of φPLPE and PY100 have been re-cut to a similar organization as Aaφ23. Gene abbreviations/functions are as follows: acylase, homoserine lactone acylase; ant, anti-repressor; atQ, anti-termination; bet, lambda recombination; BP, baseplate; cI/II, repressor; cro, anti-repressor; dnaC, replication; exo, exonuclease; H, head; hel, helicase; HNH, HNH (homing) endonuclease; hol, holin; int, integrase; lys, lysis; lyz, lysozyme; MCP, major capsid protein; meth, methylase; ninB/C/G, lambda recombination; nuc, nuclease; P, portal; pnk, polynucleotide kinase; pol, DNA polymerase; prim, primase; rec(T), recombination; recE, exonuclease VIII; rep(O/P), (λ) replication; Rz/Rz1, lysis; ssb, single-stranded binding; σ54, bacterial transcriptional regulator; T, tail; terS/L, terminase; Tu, elongation factor; tetR, bacterial transcriptional regulator; trans, transposase; V, virion; xis, excisionase.
Figure 3
Figure 3. Bipartite nature of the φPLPE group phage genomes, with variable lysogeny/replication modules and conserved structure/morphogenesis modules.
With the exception of φPLPE itself (all ORFs colored), only those ORFs shared with φPLPE in the other phages are color-coded as in Fig. 2. Shared ORFs were defined as protein matches in each phage against a φPLPE-restricted BLASTp with an E-value <10−4.
Figure 4
Figure 4. The two conserved structural mini-modules in the φPLPE group phages, excluding Aaφ23.
Color-coding is as in Fig. 2 and gene numbers refer to the φPLPE genome. ORF60 (“60″) is of unknown function, but could be implicated in the baseplate (BP). The two small ORFs upstream of the terL genes in φ1422 and ZF40 could be the terS genes. The terS/L genes in PY100 are not arranged as in the other phages and are far upstream and not side-by-side. All of the cellular hits shown are (conserved) hypothetical bacterial proteins, except for φ1422 which has a σ54 transcription regulator (“σ”).
Figure 5
Figure 5. Neighbor-joining trees of TerL (A) and portal proteins (B; φPLPE gp19 homologs).
The eight dwarf φPLPE-like myoviruses are highlighted with red arrows. Branches are colored according to phage family type: red for Myoviruses, blue for Siphoviruses, green for Podoviruses and black for unknown morphology. Values at the nodes are the results of 100 bootstrap replicates. The scale bar indicates 0.1 substitutions per site.
Figure 6
Figure 6. Whole genome similarities among φPLPE group phages.
(A) Reciprocal dot-plots of the φPLPE-like phages based on whole genome nucleotide sequences (left) or concatenations of all proteins (right). Two Mu-like and two P2-like phages have been included for comparison. (B) Similarity matrices of the DNA sequences (left) and concatenated polyproteins (right) of the phages in (A). The non-φPLPE-like phages and a randomized sequence of φPLPE serve as controls. Also included are the results of the statistical tests comparing the similarity values of the φPLPE-like phages to the controls. Similarity values are highlighted with increasingly darker shades of red.
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