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Genomic and functional analysis of Vibrio phage SIO-2 reveals novel insights into ecology and evolution of marine siphoviruses.

ABSTRACT: We report on a genomic and functional analysis of a novel marine siphovirus, the Vibrio phage SIO-2. This phage is lytic for related Vibrio species of great ecological interest including the broadly antagonistic bacterium Vibrio sp. SWAT3 as well as notable members of the Harveyi clade (V.harveyi ATTC BAA-1116 and V.campbellii ATCC 25920). Vibrio phage SIO-2 has a circularly permuted genome of 80598 bp, which displays unusual features. This genome is larger than that of most known siphoviruses and only 38 of the 116 predicted proteins had homologues in databases. Another divergence is manifest by the origin of core genes, most of which share robust similarities with unrelated viruses and bacteria spanning a wide range of phyla. These core genes are arranged in the same order as in most bacteriophages but they are unusually interspaced at two places with insertions of DNA comprising a high density of uncharacterized genes. The acquisition of these DNA inserts is associated with morphological variation of SIO-2 capsid, which assembles as a large (80 nm) shell with a novel T=12 symmetry. These atypical structural features confer on SIO-2 a remarkable stability to a variety of physical, chemical and environmental factors. Given this high level of functional and genomic novelty, SIO-2 emerges as a model of considerable interest in ecological and evolutionary studies.

SUBMITTER: Baudoux AC

PROVIDER: S-EPMC3338904 | biostudies-literature | 2012 Aug

REPOSITORIES: biostudies-literature

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Genomic and functional analysis of Vibrio phage SIO-2 reveals novel insights into ecology and evolution of marine siphoviruses.

Baudoux A-C AC Hendrix R W RW Lander G C GC Bailly X X Podell S S Paillard C C Johnson J E JE Potter C S CS Carragher B B Azam F F

Environmental microbiology 20120109 8

We report on a genomic and functional analysis of a novel marine siphovirus, the Vibrio phage SIO-2. This phage is lytic for related Vibrio species of great ecological interest including the broadly antagonistic bacterium Vibrio sp. SWAT3 as well as notable members of the Harveyi clade (V.harveyi ATTC BAA-1116 and V.campbellii ATCC 25920). Vibrio phage SIO-2 has a circularly permuted genome of 80598 bp, which displays unusual features. This genome is larger than that of most known siphoviruses a ...[more]

PMID: 22225728

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Project description:Viruses are the most abundant living entities in marine ecosystems, playing critical roles in altering the structure and function of microbial communities and driving ocean biogeochemistry. Phages that infect Roseobacter clade-affiliated (RCA) cluster strains are an important component of marine viral communities. Here, we characterize the genome sequences of two new RCA phages, CRP-9 and CRP-13, which infect RCA strain FZCC0023. Genomic analysis reveals that CRP-9 and CRP-13 represent a novel evolutionary lineage of marine phages. They both have a DNA replication module most similar to those in Cobavirus group phages. In contrast, their morphogenesis and packaging modules are distinct from those in cobaviruses but homologous to those in HMO-2011-type phages. The genomic architecture of CRP-9 and CRP-13 suggests a genomic recombination event between distinct phage groups. Metagenomic data sets were examined for metagenome-assembled viral genomes (MAVGs) with similar recombinant genome architectures. Fifteen CRP-9-type MAVGs were identified from marine viromes. Additionally, 158 MAVGs were identified containing HMO-2011-type morphogenesis and packaging modules with other types of DNA replication genes, providing more evidence that recombination between different phage groups is a major driver of phage evolution. Altogether, this study significantly expands the understanding of diversity and evolution of marine roseophages. Meanwhile, the analysis of these novel RCA phages and MAVGs highlights the critical role of recombination in shaping phage diversity. These phage sequences are valuable resources for inferring the evolutionary connection of distinct phage groups. IMPORTANCE Diversity and evolution of phages that infect the relatively slow-growing but dominant Roseobacter lineages are largely unknown. In this study, RCA phages CRP-9 and CRP-13 have been isolated on a Roseobacter RCA strain and shown to have a unique genomic architecture, which appears to be the result of a recombination event. CRP-9 and CRP-13 have a DNA replication module most similar to those in Cobavirus group phages and morphogenesis and packaging modules most similar to those in HMO-2011-type phages. HMO-2011-type morphogenesis and packaging modules are found in combination with distinct types of DNA replication genes, suggesting compatibility with various DNA replication modules. Altogether, this study contributes toward a better understanding of marine viral diversity and evolution.

Dataset Information

Genomic and functional analysis of Vibrio phage SIO-2 reveals novel insights into ecology and evolution of marine siphoviruses.

Publications

Genomic and functional analysis of Vibrio phage SIO-2 reveals novel insights into ecology and evolution of marine siphoviruses.

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