A systematic analysis of marine lysogens and proviruses

Abstract Viruses are ubiquitous in the oceans, exhibiting high abundance and diversity. Here, we systematically analyze existing genomic sequences of marine prokaryotes to compile a Marine Prokaryotic Genome Dataset (MPGD, consisting of over 12,000 bacterial and archaeal genomes) and a Marine Temper...

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Main Authors: Yi Yi, Shunzhang Liu, Yali Hao, Qingyang Sun, Xinjuan Lei, Yecheng Wang, Jiahua Wang, Mujie Zhang, Shan Tang, Qingxue Tang, Yue Zhang, Xipeng Liu, Yinzhao Wang, Xiang Xiao, Huahua Jian
Format: Article
Language:English
Published: Nature Portfolio 2023-09-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-41699-4
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author Yi Yi
Shunzhang Liu
Yali Hao
Qingyang Sun
Xinjuan Lei
Yecheng Wang
Jiahua Wang
Mujie Zhang
Shan Tang
Qingxue Tang
Yue Zhang
Xipeng Liu
Yinzhao Wang
Xiang Xiao
Huahua Jian
author_facet Yi Yi
Shunzhang Liu
Yali Hao
Qingyang Sun
Xinjuan Lei
Yecheng Wang
Jiahua Wang
Mujie Zhang
Shan Tang
Qingxue Tang
Yue Zhang
Xipeng Liu
Yinzhao Wang
Xiang Xiao
Huahua Jian
author_sort Yi Yi
collection DOAJ
description Abstract Viruses are ubiquitous in the oceans, exhibiting high abundance and diversity. Here, we systematically analyze existing genomic sequences of marine prokaryotes to compile a Marine Prokaryotic Genome Dataset (MPGD, consisting of over 12,000 bacterial and archaeal genomes) and a Marine Temperate Viral Genome Dataset (MTVGD). At least 40% of the MPGD genomes contain one or more proviral sequences, indicating that they are lysogens. The MTVGD includes over 12,900 viral contigs or putative proviruses, clustered into 10,897 viral genera. We show that lysogens and proviruses are abundant in marine ecosystems, particularly in the deep sea, and marine lysogens differ from non-lysogens in multiple genomic features and growth properties. We reveal several virus-host interaction networks of potential ecological relevance, and identify proviruses that appear to be able to infect (or to be transferred between) different bacterial classes and phyla. Auxiliary metabolic genes in the MTVGD are enriched in functions related to carbohydrate metabolism. Finally, we experimentally demonstrate the impact of a prophage on the transcriptome of a representative marine Shewanella bacterium. Our work contributes to a better understanding of the ecology of marine prokaryotes and their viruses.
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spelling doaj.art-242779a8b92342a183cf5ff18991f5d32023-11-20T09:55:59ZengNature PortfolioNature Communications2041-17232023-09-0114111510.1038/s41467-023-41699-4A systematic analysis of marine lysogens and provirusesYi Yi0Shunzhang Liu1Yali Hao2Qingyang Sun3Xinjuan Lei4Yecheng Wang5Jiahua Wang6Mujie Zhang7Shan Tang8Qingxue Tang9Yue Zhang10Xipeng Liu11Yinzhao Wang12Xiang Xiao13Huahua Jian14State Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityState Key Laboratory of Microbial Metabolism, Joint International Research Laboratory of Metabolic & Development Sciences, School of Life Sciences and Biotechnology, Shanghai Jiao Tong UniversityAbstract Viruses are ubiquitous in the oceans, exhibiting high abundance and diversity. Here, we systematically analyze existing genomic sequences of marine prokaryotes to compile a Marine Prokaryotic Genome Dataset (MPGD, consisting of over 12,000 bacterial and archaeal genomes) and a Marine Temperate Viral Genome Dataset (MTVGD). At least 40% of the MPGD genomes contain one or more proviral sequences, indicating that they are lysogens. The MTVGD includes over 12,900 viral contigs or putative proviruses, clustered into 10,897 viral genera. We show that lysogens and proviruses are abundant in marine ecosystems, particularly in the deep sea, and marine lysogens differ from non-lysogens in multiple genomic features and growth properties. We reveal several virus-host interaction networks of potential ecological relevance, and identify proviruses that appear to be able to infect (or to be transferred between) different bacterial classes and phyla. Auxiliary metabolic genes in the MTVGD are enriched in functions related to carbohydrate metabolism. Finally, we experimentally demonstrate the impact of a prophage on the transcriptome of a representative marine Shewanella bacterium. Our work contributes to a better understanding of the ecology of marine prokaryotes and their viruses.https://doi.org/10.1038/s41467-023-41699-4
spellingShingle Yi Yi
Shunzhang Liu
Yali Hao
Qingyang Sun
Xinjuan Lei
Yecheng Wang
Jiahua Wang
Mujie Zhang
Shan Tang
Qingxue Tang
Yue Zhang
Xipeng Liu
Yinzhao Wang
Xiang Xiao
Huahua Jian
A systematic analysis of marine lysogens and proviruses
Nature Communications
title A systematic analysis of marine lysogens and proviruses
title_full A systematic analysis of marine lysogens and proviruses
title_fullStr A systematic analysis of marine lysogens and proviruses
title_full_unstemmed A systematic analysis of marine lysogens and proviruses
title_short A systematic analysis of marine lysogens and proviruses
title_sort systematic analysis of marine lysogens and proviruses
url https://doi.org/10.1038/s41467-023-41699-4
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