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First Viruses Infecting the Marine Diatom Guinardia delicatula.

ABSTRACT: The marine diatom Guinardia delicatula is a cosmopolitan species that dominates seasonal blooms in the English Channel and the North Sea. Several eukaryotic parasites are known to induce the mortality of this species. Here, we report the isolation and characterization of the first viruses that infect G. delicatula. Viruses were isolated from the Western English Channel (SOMLIT-Astan station) during the late summer bloom decline of G. delicatula. A combination of laboratory approaches revealed that these lytic viruses (GdelRNAV) are small tailless particles of 35-38 nm in diameter that replicate in the host cytoplasm where both unordered particles and crystalline arrays are formed. GdelRNAV display a linear single-stranded RNA genome of ~9 kb, including two open reading frames encoding for replication and structural polyproteins. Phylogenetic relationships based on the RNA-dependent-RNA-polymerase gene marker showed that GdelRNAV are new members of the Bacillarnavirus, a monophyletic genus belonging to the order Picornavirales. GdelRNAV are specific to several strains of G. delicatula. They were rapidly and largely produced (<12 h, 9.34 × 104 virions per host cell). Our analysis points out the host's variable viral susceptibilities during the early exponential growth phase. Interestingly, we consistently failed to isolate viruses during spring and early summer while G. delicatula developed important blooms. While our study suggests that viruses do contribute to the decline of G. delicatula's late summer bloom, they may not be the primary mortality agents during the remaining blooms at SOMLIT-Astan. Future studies should focus on the relative contribution of the viral and eukaryotic pathogens to the control of Guinardia's blooms to understand the fate of these prominent organisms in marine systems.

SUBMITTER: Arsenieff L

PROVIDER: S-EPMC6334475 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description: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.

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First Viruses Infecting the Marine Diatom Guinardia delicatula.

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