Diverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage

ABSTRACT Many major marine bacterial lineages such as SAR11, Prochlorococcus, SAR116, and several Roseobacter lineages have members that are abundant, relatively slow-growing, and genome streamlined. The isolation of phages that infect SAR11 and SAR116 have demonstrated the dominance of these phages...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Zefeng Zhang, Feng Chen, Xiao Chu, Hao Zhang, Haiwei Luo, Fang Qin, Zhiqiang Zhai, Mingyu Yang, Jing Sun, Yanlin Zhao
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2019
Materias:
Acceso en línea:https://doaj.org/article/15d14ade1417467b8debfdfa2ff67ac2
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:15d14ade1417467b8debfdfa2ff67ac2
record_format dspace
spelling oai:doaj.org-article:15d14ade1417467b8debfdfa2ff67ac22021-12-02T18:39:15ZDiverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage10.1128/mSystems.00494-192379-5077https://doaj.org/article/15d14ade1417467b8debfdfa2ff67ac22019-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00494-19https://doaj.org/toc/2379-5077ABSTRACT Many major marine bacterial lineages such as SAR11, Prochlorococcus, SAR116, and several Roseobacter lineages have members that are abundant, relatively slow-growing, and genome streamlined. The isolation of phages that infect SAR11 and SAR116 have demonstrated the dominance of these phages in the marine virosphere. However, no phages have been isolated from bacteria in the Roseobacter RCA lineage, another abundant group of marine bacteria. In this study, seven RCA phages that infect three different RCA strains were isolated and characterized. All seven RCA phages belong to the Podoviridae family and have genome sizes ranging from 39.6 to 58.1 kb. Interestingly, three RCA phages (CRP-1, CRP-2, and CRP-3) show similar genomic content and architecture as SAR116 phage HMO-2011, which represents one of the most abundant known viral groups in the ocean. The high degree of homology among CRP-1, CRP-2, CRP-3, and HMO-2011 resulted in the contribution of RCA phages to the dominance of the HMO-2011-type group. CRP-4 and CRP-5 are similar to the Cobavirus group roseophages in terms of gene content and organization. The remaining two RCA phages, CRP-6 and CRP-7, show limited genomic similarity with known phages and represent two new phage groups. Metagenomic fragment recruitment analyses reveal that these RCA phage groups are much more abundant in the ocean than most existing marine roseophage groups. The characterization of these RCA phages has greatly expanded our understanding of the genomic diversity and evolution of marine roseophages and suggests the critical need for isolating phages from the abundant but “unculturable” bacteria. IMPORTANCE The RCA lineage of the marine Roseobacter group represents one of the slow-growing but dominant components of marine microbial communities. Although dozens of roseophages have been characterized, no phages infecting RCA strains have been reported. In this study, we reported on the first RCA phage genomes and investigated their distribution pattern and relative abundance in comparison with other important marine phage groups. Two of the four RCA phage groups were found closely related to previously reported SAR116 phage HMO-2011 and Cobavirus group roseophages, respectively. The remaining two groups are novel in the genome contents. Our study also revealed that RCA phages are widely distributed and exhibit high abundance in marine viromic data sets. Altogether, our findings have greatly broadened our understanding of RCA phages and emphasize the ecological and evolutionary importance of RCA phages in the marine virosphere.Zefeng ZhangFeng ChenXiao ChuHao ZhangHaiwei LuoFang QinZhiqiang ZhaiMingyu YangJing SunYanlin ZhaoAmerican Society for MicrobiologyarticleRoseobacterRCA lineageRCA phagesviromicsMicrobiologyQR1-502ENmSystems, Vol 4, Iss 6 (2019)
institution DOAJ
collection DOAJ
language EN
topic Roseobacter
RCA lineage
RCA phages
viromics
Microbiology
QR1-502
spellingShingle Roseobacter
RCA lineage
RCA phages
viromics
Microbiology
QR1-502
Zefeng Zhang
Feng Chen
Xiao Chu
Hao Zhang
Haiwei Luo
Fang Qin
Zhiqiang Zhai
Mingyu Yang
Jing Sun
Yanlin Zhao
Diverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage
description ABSTRACT Many major marine bacterial lineages such as SAR11, Prochlorococcus, SAR116, and several Roseobacter lineages have members that are abundant, relatively slow-growing, and genome streamlined. The isolation of phages that infect SAR11 and SAR116 have demonstrated the dominance of these phages in the marine virosphere. However, no phages have been isolated from bacteria in the Roseobacter RCA lineage, another abundant group of marine bacteria. In this study, seven RCA phages that infect three different RCA strains were isolated and characterized. All seven RCA phages belong to the Podoviridae family and have genome sizes ranging from 39.6 to 58.1 kb. Interestingly, three RCA phages (CRP-1, CRP-2, and CRP-3) show similar genomic content and architecture as SAR116 phage HMO-2011, which represents one of the most abundant known viral groups in the ocean. The high degree of homology among CRP-1, CRP-2, CRP-3, and HMO-2011 resulted in the contribution of RCA phages to the dominance of the HMO-2011-type group. CRP-4 and CRP-5 are similar to the Cobavirus group roseophages in terms of gene content and organization. The remaining two RCA phages, CRP-6 and CRP-7, show limited genomic similarity with known phages and represent two new phage groups. Metagenomic fragment recruitment analyses reveal that these RCA phage groups are much more abundant in the ocean than most existing marine roseophage groups. The characterization of these RCA phages has greatly expanded our understanding of the genomic diversity and evolution of marine roseophages and suggests the critical need for isolating phages from the abundant but “unculturable” bacteria. IMPORTANCE The RCA lineage of the marine Roseobacter group represents one of the slow-growing but dominant components of marine microbial communities. Although dozens of roseophages have been characterized, no phages infecting RCA strains have been reported. In this study, we reported on the first RCA phage genomes and investigated their distribution pattern and relative abundance in comparison with other important marine phage groups. Two of the four RCA phage groups were found closely related to previously reported SAR116 phage HMO-2011 and Cobavirus group roseophages, respectively. The remaining two groups are novel in the genome contents. Our study also revealed that RCA phages are widely distributed and exhibit high abundance in marine viromic data sets. Altogether, our findings have greatly broadened our understanding of RCA phages and emphasize the ecological and evolutionary importance of RCA phages in the marine virosphere.
format article
author Zefeng Zhang
Feng Chen
Xiao Chu
Hao Zhang
Haiwei Luo
Fang Qin
Zhiqiang Zhai
Mingyu Yang
Jing Sun
Yanlin Zhao
author_facet Zefeng Zhang
Feng Chen
Xiao Chu
Hao Zhang
Haiwei Luo
Fang Qin
Zhiqiang Zhai
Mingyu Yang
Jing Sun
Yanlin Zhao
author_sort Zefeng Zhang
title Diverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage
title_short Diverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage
title_full Diverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage
title_fullStr Diverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage
title_full_unstemmed Diverse, Abundant, and Novel Viruses Infecting the Marine <italic toggle="yes">Roseobacter</italic> RCA Lineage
title_sort diverse, abundant, and novel viruses infecting the marine <italic toggle="yes">roseobacter</italic> rca lineage
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/15d14ade1417467b8debfdfa2ff67ac2
work_keys_str_mv AT zefengzhang diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT fengchen diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT xiaochu diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT haozhang diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT haiweiluo diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT fangqin diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT zhiqiangzhai diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT mingyuyang diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT jingsun diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
AT yanlinzhao diverseabundantandnovelvirusesinfectingthemarineitalictoggleyesroseobacteritalicrcalineage
_version_ 1718377724141109248