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Published in: Virology Journal 1/2019

Open Access 01-12-2019 | Research

A newly isolated roseophage represents a distinct member of Siphoviridae family

Authors: Lanlan Cai, Ruijie Ma, Hong Chen, Yunlan Yang, Nianzhi Jiao, Rui Zhang

Published in: Virology Journal | Issue 1/2019

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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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Literature
2.
go back to reference Suttle CA. Marine viruses--major players in the global ecosystem. Nat Rev Microbiol. 2007;5(10):801–12.CrossRef Suttle CA. Marine viruses--major players in the global ecosystem. Nat Rev Microbiol. 2007;5(10):801–12.CrossRef
3.
go back to reference Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A, et al. Patterns and ecological drivers of ocean viral communities. Science. 2015;348(6237):1261498.CrossRef Brum JR, Ignacio-Espinoza JC, Roux S, Doulcier G, Acinas SG, Alberti A, et al. Patterns and ecological drivers of ocean viral communities. Science. 2015;348(6237):1261498.CrossRef
4.
go back to reference Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, et al. Uncovering Earth's virome. Nature. 2016;536(7617):425–30.CrossRef Paez-Espino D, Eloe-Fadrosh EA, Pavlopoulos GA, Thomas AD, Huntemann M, Mikhailova N, et al. Uncovering Earth's virome. Nature. 2016;536(7617):425–30.CrossRef
5.
go back to reference Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, et al. Abundant SAR11 viruses in the ocean. Nature. 2013;494(7437):357–60.CrossRef Zhao Y, Temperton B, Thrash JC, Schwalbach MS, Vergin KL, Landry ZC, et al. Abundant SAR11 viruses in the ocean. Nature. 2013;494(7437):357–60.CrossRef
6.
go back to reference Kang I, Oh HM, Kang D, Cho JC. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc Natl Acad Sci U S A. 2013;110(30):12343–8.CrossRef Kang I, Oh HM, Kang D, Cho JC. Genome of a SAR116 bacteriophage shows the prevalence of this phage type in the oceans. Proc Natl Acad Sci U S A. 2013;110(30):12343–8.CrossRef
7.
go back to reference Wagner-Dobler I, Biebl H. Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol. 2006;60:255–80.CrossRef Wagner-Dobler I, Biebl H. Environmental biology of the marine Roseobacter lineage. Annu Rev Microbiol. 2006;60:255–80.CrossRef
8.
go back to reference Buchan A, Gonzalez JM, Moran MA. Overview of the marine Roseobacter lineage. Appl Environ Microbiol. 2005;71(10):5665–77.CrossRef Buchan A, Gonzalez JM, Moran MA. Overview of the marine Roseobacter lineage. Appl Environ Microbiol. 2005;71(10):5665–77.CrossRef
9.
go back to reference Brinkhoff T, Giebel HA, Simon M. Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol. 2008;189(6):531–9.CrossRef Brinkhoff T, Giebel HA, Simon M. Diversity, ecology, and genomics of the Roseobacter clade: a short overview. Arch Microbiol. 2008;189(6):531–9.CrossRef
10.
go back to reference Paul JH. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J. 2008;2(6):579–89.CrossRef Paul JH. Prophages in marine bacteria: dangerous molecular time bombs or the key to survival in the seas? ISME J. 2008;2(6):579–89.CrossRef
11.
go back to reference Huang S, Zhang Y, Chen F, Jiao N. Complete genome sequence of a marine roseophage provides evidence into the evolution of gene transfer agents in alphaproteobacteria. Virol J. 2011;8:124.CrossRef Huang S, Zhang Y, Chen F, Jiao N. Complete genome sequence of a marine roseophage provides evidence into the evolution of gene transfer agents in alphaproteobacteria. Virol J. 2011;8:124.CrossRef
12.
go back to reference Zhan Y, Chen F. Bacteriophages that infect marine roseobacters: genomics and ecology. Environ Microbiol. 2019;21:1885–95.CrossRef Zhan Y, Chen F. Bacteriophages that infect marine roseobacters: genomics and ecology. Environ Microbiol. 2019;21:1885–95.CrossRef
13.
go back to reference Wagner-Dobler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J. 2010;4(1):61–77.CrossRef Wagner-Dobler I, Ballhausen B, Berger M, Brinkhoff T, Buchholz I, Bunk B, et al. The complete genome sequence of the algal symbiont Dinoroseobacter shibae: a hitchhiker's guide to life in the sea. ISME J. 2010;4(1):61–77.CrossRef
14.
go back to reference Soora M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, et al. Oxidative stress and starvation in Dinoroseobacter shibae: the role of extrachromosomal elements. Front Microbiol. 2015;6:233.CrossRef Soora M, Tomasch J, Wang H, Michael V, Petersen J, Engelen B, et al. Oxidative stress and starvation in Dinoroseobacter shibae: the role of extrachromosomal elements. Front Microbiol. 2015;6:233.CrossRef
15.
go back to reference Cai L, Yang Y, Jiao N, Zhang R. Complete genome sequence of vB_DshP-R2C, a N4-like lytic roseophage. Mar Genomics. 2015;22:15–7.CrossRef Cai L, Yang Y, Jiao N, Zhang R. Complete genome sequence of vB_DshP-R2C, a N4-like lytic roseophage. Mar Genomics. 2015;22:15–7.CrossRef
16.
go back to reference Ji JD, Zhang R, Jiao NZ. Complete genome sequence of Roseophage vB_DshP-R1, which infects Dinoroseobacter shibae DFL12. Stand Genomic Sci. 2015;10:31.CrossRef Ji JD, Zhang R, Jiao NZ. Complete genome sequence of Roseophage vB_DshP-R1, which infects Dinoroseobacter shibae DFL12. Stand Genomic Sci. 2015;10:31.CrossRef
17.
go back to reference Li BL, Zhang S, Long LJ, Huang SJ. Characterization and complete genome sequences of three N4-like Roseobacter phages isolated from the South China Sea. Curr Microbiol. 2016;73(3):409–18.CrossRef Li BL, Zhang S, Long LJ, Huang SJ. Characterization and complete genome sequences of three N4-like Roseobacter phages isolated from the South China Sea. Curr Microbiol. 2016;73(3):409–18.CrossRef
18.
go back to reference Yang Y, Cai L, Ma R, Xu Y, Tong Y, Huang Y, et al. A novel roseosiphophage isolated from the oligotrophic South China Sea. Viruses. 2017;9:109.CrossRef Yang Y, Cai L, Ma R, Xu Y, Tong Y, Huang Y, et al. A novel roseosiphophage isolated from the oligotrophic South China Sea. Viruses. 2017;9:109.CrossRef
19.
go back to reference Kutter E. Phage host range and efficiency of plating. In Bacteriophages: methods And protocols. Volume 1: isolation, characterization, and interactions. 1st edition. New York: Humana Press; 2009:141–149. Kutter E. Phage host range and efficiency of plating. In Bacteriophages: methods And protocols. Volume 1: isolation, characterization, and interactions. 1st edition. New York: Humana Press; 2009:141–149.
20.
go back to reference Middelboe M, Chan AM, Bertelsen SK. Isolation and life cycle characterization of lytic viruses infecting heterotrophic bacteria and cyanobacteria. Manual of Aquatic Viral Ecology. American Society of Limnology and Oceanography, Inc., 2010:118–33. Middelboe M, Chan AM, Bertelsen SK. Isolation and life cycle characterization of lytic viruses infecting heterotrophic bacteria and cyanobacteria. Manual of Aquatic Viral Ecology. American Society of Limnology and Oceanography, Inc., 2010:118–33.
21.
go back to reference Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18(5):821–9.CrossRef Zerbino DR, Birney E. Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18(5):821–9.CrossRef
22.
go back to reference Garneau JR, Sekulovic O, Dupuy B, Soutourina O, Monot M, Fortier LC. High prevalence and genetic diversity of large phiCD211(phiCDIF1296T)-like prophages in Clostridioides difficile. Appl Environ Microbiol. 2018;84(3):e01264–17. Garneau JR, Sekulovic O, Dupuy B, Soutourina O, Monot M, Fortier LC. High prevalence and genetic diversity of large phiCD211(phiCDIF1296T)-like prophages in Clostridioides difficile. Appl Environ Microbiol. 2018;84(3):e01264–17.
23.
go back to reference Xu Y, Zhang R, Wang N, Cai L, Tong Y, Sun Q, et al. Novel phage-host interactions and evolution as revealed by a cyanomyovirus isolated from an estuarine environment. Environ Microbiol. 2018;20(8):2974–89.CrossRef Xu Y, Zhang R, Wang N, Cai L, Tong Y, Sun Q, et al. Novel phage-host interactions and evolution as revealed by a cyanomyovirus isolated from an estuarine environment. Environ Microbiol. 2018;20(8):2974–89.CrossRef
24.
go back to reference Fokine A, Rossmann MG. Molecular architecture of tailed double-stranded DNA phages. Bacteriophage. 2014;4(1):e28281.CrossRef Fokine A, Rossmann MG. Molecular architecture of tailed double-stranded DNA phages. Bacteriophage. 2014;4(1):e28281.CrossRef
25.
go back to reference Amarillas L, Rubi-Rangel L, Chaidez C, Gonzalez-Robles A, Lightbourn-Rojas L, Leon-Felix J. Isolation and characterization of phiLLS, a novel phage with potential biocontrol agent against multidrug-resistant Escherichia coli. Front Microbiol. 2017;8:1355.CrossRef Amarillas L, Rubi-Rangel L, Chaidez C, Gonzalez-Robles A, Lightbourn-Rojas L, Leon-Felix J. Isolation and characterization of phiLLS, a novel phage with potential biocontrol agent against multidrug-resistant Escherichia coli. Front Microbiol. 2017;8:1355.CrossRef
26.
go back to reference Lang AS, Zhaxybayeva O, Beatty JT. Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol. 2012;10(7):472–82.CrossRef Lang AS, Zhaxybayeva O, Beatty JT. Gene transfer agents: phage-like elements of genetic exchange. Nat Rev Microbiol. 2012;10(7):472–82.CrossRef
27.
go back to reference Bollivar DW, Bernardoni B, Bockman MR, Miller BM, Russell DA, Delesalle VA, et al. Complete genome sequences of five bacteriophages that infect Rhodobacter capsulatus. Genome Announc. 2016;4(3):e00051–16.CrossRef Bollivar DW, Bernardoni B, Bockman MR, Miller BM, Russell DA, Delesalle VA, et al. Complete genome sequences of five bacteriophages that infect Rhodobacter capsulatus. Genome Announc. 2016;4(3):e00051–16.CrossRef
Metadata
Title
A newly isolated roseophage represents a distinct member of Siphoviridae family
Authors
Lanlan Cai
Ruijie Ma
Hong Chen
Yunlan Yang
Nianzhi Jiao
Rui Zhang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2019
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/s12985-019-1241-6

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