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A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions

Cyanophages, viruses that infect cyanobacteria, are abundant and widely distributed in aquatic ecosystems, playing important roles in regulating the abundance, activity, diversity, and evolution of cyanobacteria. A T4-like cyanophage, S-SCSM1, infecting Synechococcus and Prochlorococcus strains of d...

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Autores principales: Wang, Qiong, Cai, Lanlan, Zhang, Rui, Wei, Shuzhen, Li, Fang, Liu, Yuanfang, Xu, Yongle
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9602691/
https://www.ncbi.nlm.nih.gov/pubmed/36190421
http://dx.doi.org/10.1128/spectrum.02367-22
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author Wang, Qiong
Cai, Lanlan
Zhang, Rui
Wei, Shuzhen
Li, Fang
Liu, Yuanfang
Xu, Yongle
author_facet Wang, Qiong
Cai, Lanlan
Zhang, Rui
Wei, Shuzhen
Li, Fang
Liu, Yuanfang
Xu, Yongle
author_sort Wang, Qiong
collection PubMed
description Cyanophages, viruses that infect cyanobacteria, are abundant and widely distributed in aquatic ecosystems, playing important roles in regulating the abundance, activity, diversity, and evolution of cyanobacteria. A T4-like cyanophage, S-SCSM1, infecting Synechococcus and Prochlorococcus strains of different ecotypes, was isolated from the South China Sea in this study. For the first time, a mannose-6-phosphate isomerase (MPI) gene was identified in the cultured cyanophage. At least 11 phylogenetic clusters of cyanophage MPIs were retrieved and identified from the marine metagenomic data sets, indicating that cyanophage MPIs in the marine environment are extremely diverse. The existence of 24 genes encoding 2-oxoglutarate (2OG)-Fe(II) oxygenase superfamily proteins in the S-SCSM1 genome emphasizes their potential importance and diverse functions in reprogramming host metabolism during phage infection. Novel cell wall synthesis and modification genes found in the S-SCSM1 genome indicate that diverse phenotypic modifications imposed by phages on cyanobacterial hosts remain to be discovered. Two noncoding RNAs of cis-regulatory elements in the S-SCSM1 genome were predicted to be associated with host exopolysaccharide metabolism and photosynthesis. The isolation and genomic characterization of cyanophage S-SCSM1 provide more information on the genetic diversity of cyanophages and phage-host interactions in the marine environment. IMPORTANCE Cyanophages play important ecological roles in aquatic ecosystems. Genomic and proteomic characterizations of the T4-like cyanophage S-SCSM1 indicate that novel and diverse viral genes and phage-host interactions in the marine environment remain unexplored. The first identified mannose-6-phosphate isomerase (MPI) gene from a cultured cyanophage was found in the S-SCSM1 genome, although MPIs were previously found in viral metagenomes at high frequencies similar to those of the cyanophage photosynthetic gene psbA. The presence of 24 genes encoding 2-oxoglutarate (2OG)-Fe(II) oxygenase superfamily proteins, novel cell wall synthesis and modification genes, a nonbleaching protein A gene, and 2 noncoding RNAs of cis-regulatory elements in the S-SCSM1 genome as well as the presence of a virion-associated regulatory protein indicate the diverse functions that cyanophages have in reprogramming the metabolism and modifying the phenotypes of hosts during infection.
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spelling pubmed-96026912022-10-27 A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions Wang, Qiong Cai, Lanlan Zhang, Rui Wei, Shuzhen Li, Fang Liu, Yuanfang Xu, Yongle Microbiol Spectr Research Article Cyanophages, viruses that infect cyanobacteria, are abundant and widely distributed in aquatic ecosystems, playing important roles in regulating the abundance, activity, diversity, and evolution of cyanobacteria. A T4-like cyanophage, S-SCSM1, infecting Synechococcus and Prochlorococcus strains of different ecotypes, was isolated from the South China Sea in this study. For the first time, a mannose-6-phosphate isomerase (MPI) gene was identified in the cultured cyanophage. At least 11 phylogenetic clusters of cyanophage MPIs were retrieved and identified from the marine metagenomic data sets, indicating that cyanophage MPIs in the marine environment are extremely diverse. The existence of 24 genes encoding 2-oxoglutarate (2OG)-Fe(II) oxygenase superfamily proteins in the S-SCSM1 genome emphasizes their potential importance and diverse functions in reprogramming host metabolism during phage infection. Novel cell wall synthesis and modification genes found in the S-SCSM1 genome indicate that diverse phenotypic modifications imposed by phages on cyanobacterial hosts remain to be discovered. Two noncoding RNAs of cis-regulatory elements in the S-SCSM1 genome were predicted to be associated with host exopolysaccharide metabolism and photosynthesis. The isolation and genomic characterization of cyanophage S-SCSM1 provide more information on the genetic diversity of cyanophages and phage-host interactions in the marine environment. IMPORTANCE Cyanophages play important ecological roles in aquatic ecosystems. Genomic and proteomic characterizations of the T4-like cyanophage S-SCSM1 indicate that novel and diverse viral genes and phage-host interactions in the marine environment remain unexplored. The first identified mannose-6-phosphate isomerase (MPI) gene from a cultured cyanophage was found in the S-SCSM1 genome, although MPIs were previously found in viral metagenomes at high frequencies similar to those of the cyanophage photosynthetic gene psbA. The presence of 24 genes encoding 2-oxoglutarate (2OG)-Fe(II) oxygenase superfamily proteins, novel cell wall synthesis and modification genes, a nonbleaching protein A gene, and 2 noncoding RNAs of cis-regulatory elements in the S-SCSM1 genome as well as the presence of a virion-associated regulatory protein indicate the diverse functions that cyanophages have in reprogramming the metabolism and modifying the phenotypes of hosts during infection. American Society for Microbiology 2022-10-03 /pmc/articles/PMC9602691/ /pubmed/36190421 http://dx.doi.org/10.1128/spectrum.02367-22 Text en Copyright © 2022 Wang et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Wang, Qiong
Cai, Lanlan
Zhang, Rui
Wei, Shuzhen
Li, Fang
Liu, Yuanfang
Xu, Yongle
A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions
title A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions
title_full A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions
title_fullStr A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions
title_full_unstemmed A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions
title_short A Unique Set of Auxiliary Metabolic Genes Found in an Isolated Cyanophage Sheds New Light on Marine Phage-Host Interactions
title_sort unique set of auxiliary metabolic genes found in an isolated cyanophage sheds new light on marine phage-host interactions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9602691/
https://www.ncbi.nlm.nih.gov/pubmed/36190421
http://dx.doi.org/10.1128/spectrum.02367-22
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