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Diversity among the tailed-bacteriophages that infect the Enterobacteriaceae.

ABSTRACT: Complete genome sequences have been determined for 73 tailed-phages that infect members of the bacterial Enterobacteriaceae family. Biological criteria such as genome size, gene organization and gene orientation were used to place these phages into categories. There are 13 such categories, some of which are themselves extremely diverse. The relationships between and within these categories are discussed with an emphasis on the head assembly genes. Although some of them are clearly homologues, suggesting a very ancient origin, there is little evidence for exchange of individual head genes between these phage categories. More recent horizontal exchange of phage tail fiber and early proteins between the categories occurs, but is probably not extremely rapid.

SUBMITTER: Casjens SR

PROVIDER: S-EPMC2607141 | biostudies-literature | 2008 Jun

REPOSITORIES: biostudies-literature

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Diversity among the tailed-bacteriophages that infect the Enterobacteriaceae.

Casjens Sherwood R SR

Research in microbiology 20080430 5

Complete genome sequences have been determined for 73 tailed-phages that infect members of the bacterial Enterobacteriaceae family. Biological criteria such as genome size, gene organization and gene orientation were used to place these phages into categories. There are 13 such categories, some of which are themselves extremely diverse. The relationships between and within these categories are discussed with an emphasis on the head assembly genes. Although some of them are clearly homologues, su ...[more]

PMID: 18550341

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Project description:The marine methylotrophic OM43 clade is considered an important bacterial group in coastal microbial communities. OM43 bacteria, which are closely related to phytoplankton blooms, have small cell sizes and streamlined genomes. Bacteriophages profoundly shape the evolutionary trajectories, population dynamics, and physiology of microbes. The prevalence and diversity of several phages that infect OM43 bacteria have been reported. In this study, we isolated and sequenced two novel OM43 phages, MEP401 and MEP402. These phages share 90% of their open reading frames (ORFs) and are distinct from other known phage isolates. Furthermore, a total of 99 metagenomic viral genomes (MVGs) closely related to MEP401 and MEP402 were identified. Phylogenomic analyses suggest that MEP401, MEP402, and these identified MVGs belong to a novel subfamily in the family Zobellviridae and that they can be separated into two groups. Group I MVGs show conserved whole-genome synteny with MEP401, while group II MVGs possess the MEP401-type DNA replication module and a distinct type of morphogenesis and packaging module, suggesting that genomic recombination occurred between phages. Most members in these two groups were predicted to infect OM43 bacteria. Metagenomic read-mapping analysis revealed that the phages in these two groups are globally ubiquitous and display distinct biogeographic distributions, with some phages being predominant in cold regions, some exclusively detected in estuarine stations, and others displaying wider distributions. This study expands our knowledge of the diversity and ecology of a novel phage lineage that infects OM43 bacteria by describing their genomic diversity and global distribution patterns. IMPORTANCE OM43 phages that infect marine OM43 bacteria are important for host mortality, community structure, and physiological functions. In this study, two OM43 phages were isolated and characterized. Metagenomic viral genome (MVG) retrieval using these two OM43 phages as baits led to the identification of two phage groups of a new subfamily in the family Zobellviridae. We found that group I MVGs share similar genomic content and arrangement with MEP401 and MEP402, whereas group II MVGs only possess the MEP401-type DNA replication module. Metagenomic mapping analysis suggests that members in these two groups are globally ubiquitous with distinct distribution patterns. This study provides important insights into the genomic diversity and biogeography of the OM43 phages in the global ocean.

Project description:BACKGROUND: The genetic diversity observed among bacteriophages remains a major obstacle for the identification of homologs and the comparison of their functional modules. In the structural module, although several classes of homologous proteins contributing to the head and tail structure can be detected, proteins of the head-to-tail connection (or neck) are generally more divergent. Yet, molecular analyses of a few tailed phages belonging to different morphological classes suggested that only a limited number of structural solutions are used in order to produce a functional virion. To challenge this hypothesis and analyze proteins diversity at the virion neck, we developed a specific computational strategy to cope with sequence divergence in phage proteins. We searched for homologs of a set of proteins encoded in the structural module using a phage learning database. RESULTS: We show that using a combination of iterative profile-profile comparison and gene context analyses, we can identify a set of head, neck and tail proteins in most tailed bacteriophages of our database. Classification of phages based on neck protein sequences delineates 4 Types corresponding to known morphological subfamilies. Further analysis of the most abundant Type 1 yields 10 Clusters characterized by consistent sets of head, neck and tail proteins. We developed Virfam, a webserver that automatically identifies proteins of the phage head-neck-tail module and assign phages to the most closely related cluster of phages. This server was tested against 624 new phages from the NCBI database. 93% of the tailed and unclassified phages could be assigned to our head-neck-tail based categories, thus highlighting the large representativeness of the identified virion architectures. Types and Clusters delineate consistent subgroups of Caudovirales, which correlate with several virion properties. CONCLUSIONS: Our method and webserver have the capacity to automatically classify most tailed phages, detect their structural module, assign a function to a set of their head, neck and tail genes, provide their morphologic subtype and localize these phages within a "head-neck-tail" based classification. It should enable analysis of large sets of phage genomes. In particular, it should contribute to the classification of the abundant unknown viruses found on assembled contigs of metagenomic samples.

Dataset Information

Diversity among the tailed-bacteriophages that infect the Enterobacteriaceae.

Publications

Diversity among the tailed-bacteriophages that infect the Enterobacteriaceae.

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