Genome Analysis of Two Novel Synechococcus Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of Cyanomyoviruses.

Tong Jiang,Hongbing Shao,Cui Guo,Min Wang,Yantao Liang,Meiwen Wang,Xinran Zhang,Andrew Mcminn,Hui He,Yundan Liu,Yong Jiang

doi:10.3390/v12080800

Abstract

The abundant and widespread unicellular cyanobacteria Synechococcus plays an important role in contributing to global phytoplankton primary production. In the present study, two novel cyanomyoviruses, S-N03 and S-H34 that infected Synechococcus MW02, were isolated from the coastal waters of the Yellow Sea. S-N03 contained a 167,069-bp genome comprising double-stranded DNA with a G + C content of 50.1%, 247 potential open reading frames and 1 tRNA; S-H34 contained a 167,040-bp genome with a G + C content of 50.1%, 246 potential open reading frames and 5 tRNAs. These two cyanophages contain fewer auxiliary metabolic genes (AMGs) than other previously isolated cyanophages. S-H34 in particular, is currently the only known cyanomyovirus that does not contain any AMGs related to photosynthesis. The absence of such common AMGs in S-N03 and S-H34, their distinct evolutionary history and ecological features imply that the energy for phage production might be obtained from other sources rather than being strictly dependent on the maintenance of photochemical ATP under high light. Phylogenetic analysis showed that the two isolated cyanophages clustered together and had a close relationship with two other cyanophages of low AMG content. Comparative genomic analysis, habitats and hosts across 81 representative cyanomyovirus showed that cyanomyovirus with less AMGs content all belonged to Synechococcus phages isolated from eutrophic waters. The relatively small genome size and high G + C content may also relate to the lower AMG content, as suggested by the significant correlation between the number of AMGs and G + C%. Therefore, the lower content of AMG in S-N03 and S-H34 might be a result of viral evolution that was likely shaped by habitat, host, and their genomic context. The genomic content of AMGs in cyanophages may have adaptive significance and provide clues to their evolution.

Highlights

With cell numbers of up to 106 cells mL−1 in the global oceans, unicellular cyanobacteria are amongst the most abundant photosynthetic organisms on earth and make major contributions to Viruses 2020, 12, 800; doi:10.3390/v12080800 www.mdpi.com/journal/virusesViruses 2020, 12, 800 marine phytoplankton primary production [1,2]
All known marine cyanophages are tailed double-stranded DNA viruses belonging to three well-defined bacteriophage families, Myoviridae, Podoviridae, and Siphoviridae [5]
The cross-infectivity test showed that both S-N03 and S-H34 infected the other three PE-type Synechococcuses belonging to subcluster 5.1 clade II, V and subcluster 5.2 (Table S1)

Summary

Introduction

With cell numbers of up to 106 cells mL−1 in the global oceans, unicellular cyanobacteria are amongst the most abundant photosynthetic organisms on earth and make major contributions to Viruses 2020, 12, 800; doi:10.3390/v12080800 www.mdpi.com/journal/virusesViruses 2020, 12, 800 marine phytoplankton primary production [1,2]. With cell numbers of up to 106 cells mL−1 in the global oceans, unicellular cyanobacteria are amongst the most abundant photosynthetic organisms on earth and make major contributions to Viruses 2020, 12, 800; doi:10.3390/v12080800 www.mdpi.com/journal/viruses. Synechococcus and Prochlorococcus, the two most common marine cyanobacteria, are responsible for roughly one half of marine photosynthesis and are key players in marine biogeochemical cycles [2,3,4]. Cyanophages are viruses that infect cyanobacteria and make up an extremely abundant and genetically diverse component of marine planktonic communities. Cyanophage infection is responsible for the mortality of a significant proportion of all cyanobacteria [6], regulating both their abundance and diversity. More than 80% of Synechococcus cells were estimated to encounter infectious cyanophages on a daily basis, and ~5% to 7% of cells would become infected by viruses [6]. Viral lysis of host cells channel, or “shunt”, the photosynthetically-fixed carbon (particulate organic matter, POM) to the dissolved organic matter (DOM) pool that can be reused by cyanobacteria, driving recycling [7]

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Results

Conclusion