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A Novel Benthic Phage Infecting Shewanella with Strong Replication Ability.

ABSTRACT: The coastal sediments were considered to contain diverse phages playing important roles in driving biogeochemical cycles based on genetic analysis. However, till now, benthic phages in coastal sediments were very rarely isolated, which largely limits our understanding of their biological characteristics. Here, we describe a novel lytic phage (named Shewanella phage S0112) isolated from the coastal sediments of the Yellow Sea infecting a sediment bacterium of the genus Shewanella. The phage has a very high replication capability, with the burst size of ca. 1170 phage particles per infected cell, which is 5-10 times higher than that of most phages isolated before. Meanwhile, the latent period of this phage is relatively longer, which might ensure adequate time for phage replication. The phage has a double-stranded DNA genome comprising 62,286 bp with 102 ORFs, ca. 60% of which are functionally unknown. The expression products of 16 ORF genes, mainly structural proteins, were identified by LC-MS/MS analysis. Besides the general DNA metabolism and structure assembly genes in the phage genome, there is a cluster of auxiliary metabolic genes that may be involved in 7-cyano-7-deazaguanine (preQ₀) biosynthesis. Meanwhile, a pyrophosphohydrolase (MazG) gene being considered as a regulator of programmed cell death or involving in host stringer responses is inserted in this gene cluster. Comparative genomic and phylogenetic analysis both revealed a great novelty of phage S0112. This study represents the first report of a benthic phage infecting Shewanella, which also sheds light on the phage-host interactions in coastal sediments.

SUBMITTER: Wang Z

PROVIDER: S-EPMC6893657 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Bacteriophages play critical roles in impacting microbial community succession both ecologically and evolutionarily. Although the majority of phage genetic diversity has been increasingly unveiled, phages infecting members of the ecologically important genus Alteromonas remain poorly understood. Here, we present a comprehensive analysis of a newly isolated alterophage, vB_AcoS-R7M (R7M), to characterize its life cycle traits, genomic features, and putative evolutionary origin. R7M harbors abundant genes identified as host-like auxiliary metabolic genes facilitating viral propagation. Genomic analysis suggested that R7M is distinct from currently known alterophages. Interestingly, R7M was found to share a set of similar characteristics with a number of siphophages infecting diverse aquatic opportunistic copiotrophs. We therefore proposed the creation of one new subfamily (Queuovirinae) to group with these evolutionarily related phages. Notably, tail genes were less likely to be shared among them, and baseplate-related genes varied the most. In-depth analyses indicated that R7M has replaced its distal tail with a Rhodobacter capsulatus gene transfer agent (RcGTA)-like baseplate and further acquired a putative receptor interaction site targeting Alteromonas. These findings suggest that horizontal exchanges of viral tail adsorption apparatuses are widespread and vital for phages to hunt new hosts and to adapt to new niches. IMPORTANCE The evolution and ecology of phages infecting members of Alteromonas, a marine opportunistic genus that is widely distributed and of great ecological significance, remain poorly understood. The present study integrates physiological and genomic evidence to characterize the properties and putative phage-host interactions of a newly isolated Alteromonas phage, vB_AcoS-R7M (R7M). A taxonomic study reveals close evolutionary relationships among R7M and a number of siphophages infecting various aquatic copiotrophs. Their similar head morphology and overall genetic framework suggest their putative common ancestry and the grouping of a new viral subfamily. However, their major difference lies in the viral tail adsorption apparatuses and the horizontal exchanges of which possibly account for variations in host specificity. These findings outline an evolutionary scenario for the emergence of diverse viral lineages of a shared genetic pool and give insights into the genetics and ecology of viral host jumps.

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A Novel Benthic Phage Infecting Shewanella with Strong Replication Ability.

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