A newly isolated roseophage represents a distinct member of Siphoviridae family

Abstract Background Members of the Roseobacter lineage are a major group of marine heterotrophic bacteria because of their wide distribution, versatile lifestyles and important biogeochemical roles. Bacteriophages, the most abundant biological entities in the ocean, play important roles in shaping t...

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Main Authors: Lanlan Cai, Ruijie Ma, Hong Chen, Yunlan Yang, Nianzhi Jiao, Rui Zhang
Format: Article
Language:English
Published: BMC 2019-11-01
Series:Virology Journal
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12985-019-1241-6
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author Lanlan Cai
Ruijie Ma
Hong Chen
Yunlan Yang
Nianzhi Jiao
Rui Zhang
author_facet Lanlan Cai
Ruijie Ma
Hong Chen
Yunlan Yang
Nianzhi Jiao
Rui Zhang
author_sort Lanlan Cai
collection DOAJ
description Abstract Background Members of the Roseobacter lineage are a major group of marine heterotrophic bacteria because of their wide distribution, versatile lifestyles and important biogeochemical roles. Bacteriophages, the most abundant biological entities in the ocean, play important roles in shaping their hosts’ population structures and mediating genetic exchange between hosts. However, our knowledge of roseophages (bacteriophages that infect Roseobacter) is far behind that of their host counterparts, partly reflecting the need to isolate and analyze the phages associated with this ecologically important bacterial clade. Methods vB_DshS-R4C (R4C), a novel virulent roseophage that infects Dinoroseobacter shibae DFL12T, was isolated with the double-layer agar method. The phage morphology was visualized with transmission electron microscopy. We characterized R4C in-depth with a genomic analysis and investigated the distribution of the R4C genome in different environments with a metagenomic recruitment analysis. Results The double-stranded DNA genome of R4C consists of 36,291 bp with a high GC content of 66.75%. It has 49 genes with low DNA and protein homologies to those of other known phages. Morphological and phylogenetic analyses suggested that R4C is a novel member of the family Siphoviridae and is most closely related to phages in the genus Cronusvirus. However, unlike the Cronusvirus phages, R4C encodes an integrase, implying its ability to establish a lysogenic life cycle. A terminal analysis shows that, like that of λ phage, the R4C genome utilize the ‘cohesive ends’ DNA-packaging mechanism. Significantly, homologues of the R4C genes are more prevalent in coastal areas than in the open ocean. Conclusions Information about this newly discovered phage extends our understanding of bacteriophage diversity, evolution, and their roles in different environments.
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spelling doaj.art-b8419e9e996f41c4a0f4433a7e57be7a2022-12-22T00:36:35ZengBMCVirology Journal1743-422X2019-11-011611910.1186/s12985-019-1241-6A newly isolated roseophage represents a distinct member of Siphoviridae familyLanlan Cai0Ruijie Ma1Hong Chen2Yunlan Yang3Nianzhi Jiao4Rui Zhang5State Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen UniversityState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen UniversityState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen UniversityState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen UniversityState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen UniversityState Key Laboratory of Marine Environmental Science, College of Ocean and Earth Sciences, Institute of Marine Microbes and Ecospheres, Xiamen UniversityAbstract Background Members of the Roseobacter lineage are a major group of marine heterotrophic bacteria because of their wide distribution, versatile lifestyles and important biogeochemical roles. Bacteriophages, the most abundant biological entities in the ocean, play important roles in shaping their hosts’ population structures and mediating genetic exchange between hosts. However, our knowledge of roseophages (bacteriophages that infect Roseobacter) is far behind that of their host counterparts, partly reflecting the need to isolate and analyze the phages associated with this ecologically important bacterial clade. Methods vB_DshS-R4C (R4C), a novel virulent roseophage that infects Dinoroseobacter shibae DFL12T, was isolated with the double-layer agar method. The phage morphology was visualized with transmission electron microscopy. We characterized R4C in-depth with a genomic analysis and investigated the distribution of the R4C genome in different environments with a metagenomic recruitment analysis. Results The double-stranded DNA genome of R4C consists of 36,291 bp with a high GC content of 66.75%. It has 49 genes with low DNA and protein homologies to those of other known phages. Morphological and phylogenetic analyses suggested that R4C is a novel member of the family Siphoviridae and is most closely related to phages in the genus Cronusvirus. However, unlike the Cronusvirus phages, R4C encodes an integrase, implying its ability to establish a lysogenic life cycle. A terminal analysis shows that, like that of λ phage, the R4C genome utilize the ‘cohesive ends’ DNA-packaging mechanism. Significantly, homologues of the R4C genes are more prevalent in coastal areas than in the open ocean. Conclusions Information about this newly discovered phage extends our understanding of bacteriophage diversity, evolution, and their roles in different environments.http://link.springer.com/article/10.1186/s12985-019-1241-6DinoroseobacterRoseophageSiphoviridaeGenome sequence
spellingShingle Lanlan Cai
Ruijie Ma
Hong Chen
Yunlan Yang
Nianzhi Jiao
Rui Zhang
A newly isolated roseophage represents a distinct member of Siphoviridae family
Virology Journal
Dinoroseobacter
Roseophage
Siphoviridae
Genome sequence
title A newly isolated roseophage represents a distinct member of Siphoviridae family
title_full A newly isolated roseophage represents a distinct member of Siphoviridae family
title_fullStr A newly isolated roseophage represents a distinct member of Siphoviridae family
title_full_unstemmed A newly isolated roseophage represents a distinct member of Siphoviridae family
title_short A newly isolated roseophage represents a distinct member of Siphoviridae family
title_sort newly isolated roseophage represents a distinct member of siphoviridae family
topic Dinoroseobacter
Roseophage
Siphoviridae
Genome sequence
url http://link.springer.com/article/10.1186/s12985-019-1241-6
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