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

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 ?1422, 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.

SUBMITTER: Comeau AM

PROVIDER: S-EPMC3391216 | biostudies-literature | 2012

REPOSITORIES: biostudies-literature

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

Comeau André M AM Tremblay Denise D Moineau Sylvain S Rattei Thomas T Kushkina Alla I AI Tovkach Fedor I FI Krisch Henry M HM Ackermann Hans-Wolfgang HW

PloS one 20120706 7

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 t ...[more]

PMID: 22792219

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Project description:BackgroundThe recently sequenced 218 kb genome of morphologically atypical Bacillus thuringiensis phage 0305phi8-36 exhibited only limited detectable homology to known bacteriophages. The only known relative of this phage is a string of phage-like genes called BtI1 in the chromosome of B. thuringiensis israelensis. The high degree of divergence and novelty of phage genomes pose challenges in how to describe the phage from its genomic sequences.ResultsPhage 0305phi8-36 and BtI1 are estimated to have diverged 2.0 - 2.5 billion years ago. Positionally biased Blast searches aligned 30 homologous structure or morphogenesis genes between 0305phi8-36 and BtI1 that have maintained the same gene order. Functional clustering of the genes helped identify additional gene functions. A conserved long tape measure gene indicates that a long tail is an evolutionarily stable property of this phage lineage. An unusual form of the tail chaperonin system split to two genes was characterized, as was a hyperplastic homologue of the T4gp27 hub gene. Within this region some segments were best described as encoding a conservative array of structure domains fused with a variable component of exchangeable domains. Other segments were best described as multigene units engaged in modular horizontal exchange. The non-structure genes of 0305phi8-36 appear to include the remnants of two replicative systems leading to the hypothesis that the genome plan was created by fusion of two ancestral viruses. The case for a member of the RNAi RNA-directed RNA polymerase family residing in 0305phi8-36 was strengthened by extending the hidden Markov model of this family. Finally, it was noted that prospective transcriptional promoters were distributed in a gradient of small to large transcripts starting from a fixed end of the genome.ConclusionGenomic organization at a level higher than individual gene sequence comparison can be analyzed to aid in understanding large phage genomes. Methods of analysis include 1) applying a time scale, 2) augmenting blast scores with positional information, 3) categorizing genomic rearrangements into one of several processes with characteristic rates and outcomes, and 4) correlating apparent transcript sizes with genomic position, gene content, and promoter motifs.

Project description:Cotton is one of the most economically important fiber crop plants worldwide. The genus Gossypium contains a single allotetraploid group (AD) and eight diploid genome groups (A-G and K). However, the evolution of repeat sequences in the chloroplast genomes and the phylogenetic relationships of Gossypium species are unclear. Thus, we determined the variations in the repeat sequences and the evolutionary relationships of 40 cotton chloroplast genomes, which represented the most diverse in the genus, including five newly sequenced diploid species, i.e., G. nandewarense (C1-n), G. armourianum (D2-1), G. lobatum (D7), G. trilobum (D8), and G. schwendimanii (D11), and an important semi-wild race of upland cotton, G. hirsutum race latifolium (AD1). The genome structure, gene order, and GC content of cotton species were similar to those of other higher plant plastid genomes. In total, 2860 long sequence repeats (>10 bp in length) were identified, where the F-genome species had the largest number of repeats (G. longicalyx F1: 108) and E-genome species had the lowest (G. stocksii E1: 53). Large-scale repeat sequences possibly enrich the genetic information and maintain genome stability in cotton species. We also identified 10 divergence hotspot regions, i.e., rpl33-rps18, psbZ-trnG (GCC), rps4-trnT (UGU), trnL (UAG)-rpl32, trnE (UUC)-trnT (GGU), atpE, ndhI, rps2, ycf1, and ndhF, which could be useful molecular genetic markers for future population genetics and phylogenetic studies. Site-specific selection analysis showed that some of the coding sites of 10 chloroplast genes (atpB, atpE, rps2, rps3, petB, petD, ccsA, cemA, ycf1, and rbcL) were under protein sequence evolution. Phylogenetic analysis based on the whole plastomes suggested that the Gossypium species grouped into six previously identified genetic clades. Interestingly, all 13 D-genome species clustered into a strong monophyletic clade. Unexpectedly, the cotton species with C, G, and K-genomes were admixed and nested in a large clade, which could have been due to their recent radiation, incomplete lineage sorting, and introgression hybridization among different cotton lineages. In conclusion, the results of this study provide new insights into the evolution of repeat sequences in chloroplast genomes and interspecific relationships in the genus Gossypium.

Dataset Information

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

Publications

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

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