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

The abundant and widespread unicellular cyanobacteria <i>Synechococcus</i> 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 <i>Synechococcus</i> MW02, were isolat...

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Main Authors: Tong Jiang, Cui Guo, Min Wang, Meiwen Wang, Xinran Zhang, Yundan Liu, Yantao Liang, Yong Jiang, Hui He, Hongbing Shao, Andrew McMinn
Format: Article
Language:English
Published: MDPI AG 2020-07-01
Series:Viruses
Subjects:
Online Access:https://www.mdpi.com/1999-4915/12/8/800
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author Tong Jiang
Cui Guo
Min Wang
Meiwen Wang
Xinran Zhang
Yundan Liu
Yantao Liang
Yong Jiang
Hui He
Hongbing Shao
Andrew McMinn
author_facet Tong Jiang
Cui Guo
Min Wang
Meiwen Wang
Xinran Zhang
Yundan Liu
Yantao Liang
Yong Jiang
Hui He
Hongbing Shao
Andrew McMinn
author_sort Tong Jiang
collection DOAJ
description The abundant and widespread unicellular cyanobacteria <i>Synechococcus</i> 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 <i>Synechococcus</i> 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 <i>Synechococcus</i> 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.
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spelling doaj.art-1190d79fe29e4ae89b95720d997413122023-11-20T07:57:39ZengMDPI AGViruses1999-49152020-07-0112880010.3390/v12080800Genome Analysis of Two Novel <i>Synechococcus</i> Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of CyanomyovirusesTong Jiang0Cui Guo1Min Wang2Meiwen Wang3Xinran Zhang4Yundan Liu5Yantao Liang6Yong Jiang7Hui He8Hongbing Shao9Andrew McMinn10College of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaCollege of Marine Life Sciences, Ocean University of China, Qingdao 266003, ChinaThe abundant and widespread unicellular cyanobacteria <i>Synechococcus</i> 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 <i>Synechococcus</i> 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 <i>Synechococcus</i> 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.https://www.mdpi.com/1999-4915/12/8/800cyanophage<i>Myoviridae</i>AMGsgenomephotosynthesis
spellingShingle Tong Jiang
Cui Guo
Min Wang
Meiwen Wang
Xinran Zhang
Yundan Liu
Yantao Liang
Yong Jiang
Hui He
Hongbing Shao
Andrew McMinn
Genome Analysis of Two Novel <i>Synechococcus</i> Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of Cyanomyoviruses
Viruses
cyanophage
<i>Myoviridae</i>
AMGs
genome
photosynthesis
title Genome Analysis of Two Novel <i>Synechococcus</i> Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of Cyanomyoviruses
title_full Genome Analysis of Two Novel <i>Synechococcus</i> Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of Cyanomyoviruses
title_fullStr Genome Analysis of Two Novel <i>Synechococcus</i> Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of Cyanomyoviruses
title_full_unstemmed Genome Analysis of Two Novel <i>Synechococcus</i> Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of Cyanomyoviruses
title_short Genome Analysis of Two Novel <i>Synechococcus</i> Phages That Lack Common Auxiliary Metabolic Genes: Possible Reasons and Ecological Insights by Comparative Analysis of Cyanomyoviruses
title_sort genome analysis of two novel i synechococcus i phages that lack common auxiliary metabolic genes possible reasons and ecological insights by comparative analysis of cyanomyoviruses
topic cyanophage
<i>Myoviridae</i>
AMGs
genome
photosynthesis
url https://www.mdpi.com/1999-4915/12/8/800
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