Identification of hidden N4-like viruses and their interactions with hosts
ABSTRACT The N4-like viruses, which were recently assigned to the novel viral family Schitoviridae in 2021, belong to a podoviral-like viral lineage and possess conserved genomic characteristics and a unique replication mechanism. Despite their significance, our understanding of N4-like viruses is p...
| Main Authors: | , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
American Society for Microbiology
2023-10-01
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| Series: | mSystems |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/msystems.00197-23 |
| _version_ | 1797617639494778880 |
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| author | Kaiyang Zheng Yantao Liang David Paez-Espino Xiao Zou Chen Gao Hongbing Shao Yeong Yik Sung Wen Jye Mok Li Lian Wong Yu-Zhong Zhang Jiwei Tian Feng Chen Nianzhi Jiao Curtis A. Suttle Jianfeng He Andrew McMinn Min Wang |
| author_facet | Kaiyang Zheng Yantao Liang David Paez-Espino Xiao Zou Chen Gao Hongbing Shao Yeong Yik Sung Wen Jye Mok Li Lian Wong Yu-Zhong Zhang Jiwei Tian Feng Chen Nianzhi Jiao Curtis A. Suttle Jianfeng He Andrew McMinn Min Wang |
| author_sort | Kaiyang Zheng |
| collection | DOAJ |
| description | ABSTRACT The N4-like viruses, which were recently assigned to the novel viral family Schitoviridae in 2021, belong to a podoviral-like viral lineage and possess conserved genomic characteristics and a unique replication mechanism. Despite their significance, our understanding of N4-like viruses is primarily based on viral isolates. To address this knowledge gap, this study has established a comprehensive N4-like viral data sets comprising 342 high-quality N4-like viruses/proviruses (144 viral isolates, 158 uncultured viruses, and 40 integrated N4-like proviruses). These viruses were classified into 97 subfamilies (89 of which are newly identified), 148 genera (100 of which are newly identified), and 253 species (177 of which are newly identified). The study reveals that N4-like viruses inhibit the polar region, oligotrophic open oceans, and the human gut, where they infect various bacterial lineages, such as Alpha/Beta/Gamma/Epsilon-proteobacteria in the Proteobacteria phylum. Although N4-like viral endogenization appears to be prevalent in Proteobacteria, it has also been observed in Firmicutes. Additionally, the phylogenetic analysis has identified evolutionary divergence within the hallmark genes of N4-like viruses, indicating a complex origin of the different conserved parts of viral genomes. Moreover, 1,101 putative auxiliary metabolic genes (AMGs) were identified in the N4-like viral pan-proteome, which mainly participate in nucleotide and cofactor/vitamin metabolisms. Of these AMGs, 27 were found to be associated with virulence, suggesting their potential involvement in the spread of bacterial pathogenicity. Importance The findings of this study are significant, as N4-like viruses represent a unique viral lineage with a distinct replication mechanism and a conserved core genome. This work has resulted in a comprehensive global map of the entire N4-like viral lineage, including information on their distribution in different biomes, evolutionary divergence, genomic diversity, and the potential for viral-mediated host metabolic reprogramming. As such, this work significantly contributes to our understanding of the ecological function and viral-host interactions of bacteriophages. |
| first_indexed | 2024-03-11T07:58:42Z |
| format | Article |
| id | doaj.art-5872a4c80455465fb8e150ea55bcd49c |
| institution | Directory Open Access Journal |
| issn | 2379-5077 |
| language | English |
| last_indexed | 2024-03-11T07:58:42Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | mSystems |
| spelling | doaj.art-5872a4c80455465fb8e150ea55bcd49c2023-11-17T03:22:37ZengAmerican Society for MicrobiologymSystems2379-50772023-10-018510.1128/msystems.00197-23Identification of hidden N4-like viruses and their interactions with hostsKaiyang Zheng0Yantao Liang1David Paez-Espino2Xiao Zou3Chen Gao4Hongbing Shao5Yeong Yik Sung6Wen Jye Mok7Li Lian Wong8Yu-Zhong Zhang9Jiwei Tian10Feng Chen11Nianzhi Jiao12Curtis A. Suttle13Jianfeng He14Andrew McMinn15Min Wang16Key Laboratory of Polar Oceanography and Global Ocean Change, Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, ChinaKey Laboratory of Polar Oceanography and Global Ocean Change, Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, ChinaDOE Joint Genome Institute, Lawrence Berkeley National Laboratory , Berkeley, California, USAQingdao Central Hospital , Qingdao, ChinaKey Laboratory of Polar Oceanography and Global Ocean Change, Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, ChinaKey Laboratory of Polar Oceanography and Global Ocean Change, Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, ChinaUMT-OUC Joint Centre for Marine Studies , Qingdao, ChinaUMT-OUC Joint Centre for Marine Studies , Qingdao, ChinaUMT-OUC Joint Centre for Marine Studies , Qingdao, ChinaKey Laboratory of Polar Oceanography and Global Ocean Change, Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, ChinaKey Laboratory of Physical Oceanography, Ministry of Education, Ocean University of China , Qingdao, ChinaInstitute of Marine and Environmental Technology, University of Maryland Center for Environmental Science , Baltimore, Maryland, USAState Key Laboratory of Marine Environmental Sciences, Institute of Marine Microbes and Ecospheres, Xiamen University , Xiamen, ChinaDepartment of Earth, Ocean and Atmospheric Sciences, Institute for the Oceans and Fisheries, The University of British Columbia , Vancouver, British Columbia, CanadaSOA Key Laboratory for Polar Science, Polar Research Institute of China , Shanghai, ChinaKey Laboratory of Polar Oceanography and Global Ocean Change, Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, ChinaKey Laboratory of Polar Oceanography and Global Ocean Change, Frontiers Science Center for Deep Ocean Multispheres and Earth System, College of Marine Life Sciences, Institute of Evolution and Marine Biodiversity, Ocean University of China , Qingdao, ChinaABSTRACT The N4-like viruses, which were recently assigned to the novel viral family Schitoviridae in 2021, belong to a podoviral-like viral lineage and possess conserved genomic characteristics and a unique replication mechanism. Despite their significance, our understanding of N4-like viruses is primarily based on viral isolates. To address this knowledge gap, this study has established a comprehensive N4-like viral data sets comprising 342 high-quality N4-like viruses/proviruses (144 viral isolates, 158 uncultured viruses, and 40 integrated N4-like proviruses). These viruses were classified into 97 subfamilies (89 of which are newly identified), 148 genera (100 of which are newly identified), and 253 species (177 of which are newly identified). The study reveals that N4-like viruses inhibit the polar region, oligotrophic open oceans, and the human gut, where they infect various bacterial lineages, such as Alpha/Beta/Gamma/Epsilon-proteobacteria in the Proteobacteria phylum. Although N4-like viral endogenization appears to be prevalent in Proteobacteria, it has also been observed in Firmicutes. Additionally, the phylogenetic analysis has identified evolutionary divergence within the hallmark genes of N4-like viruses, indicating a complex origin of the different conserved parts of viral genomes. Moreover, 1,101 putative auxiliary metabolic genes (AMGs) were identified in the N4-like viral pan-proteome, which mainly participate in nucleotide and cofactor/vitamin metabolisms. Of these AMGs, 27 were found to be associated with virulence, suggesting their potential involvement in the spread of bacterial pathogenicity. Importance The findings of this study are significant, as N4-like viruses represent a unique viral lineage with a distinct replication mechanism and a conserved core genome. This work has resulted in a comprehensive global map of the entire N4-like viral lineage, including information on their distribution in different biomes, evolutionary divergence, genomic diversity, and the potential for viral-mediated host metabolic reprogramming. As such, this work significantly contributes to our understanding of the ecological function and viral-host interactions of bacteriophages.https://journals.asm.org/doi/10.1128/msystems.00197-23N4-like virusesgenomediversityevolutionary divergenceviral-mediated host metabolic reprogramming |
| spellingShingle | Kaiyang Zheng Yantao Liang David Paez-Espino Xiao Zou Chen Gao Hongbing Shao Yeong Yik Sung Wen Jye Mok Li Lian Wong Yu-Zhong Zhang Jiwei Tian Feng Chen Nianzhi Jiao Curtis A. Suttle Jianfeng He Andrew McMinn Min Wang Identification of hidden N4-like viruses and their interactions with hosts mSystems N4-like viruses genome diversity evolutionary divergence viral-mediated host metabolic reprogramming |
| title | Identification of hidden N4-like viruses and their interactions with hosts |
| title_full | Identification of hidden N4-like viruses and their interactions with hosts |
| title_fullStr | Identification of hidden N4-like viruses and their interactions with hosts |
| title_full_unstemmed | Identification of hidden N4-like viruses and their interactions with hosts |
| title_short | Identification of hidden N4-like viruses and their interactions with hosts |
| title_sort | identification of hidden n4 like viruses and their interactions with hosts |
| topic | N4-like viruses genome diversity evolutionary divergence viral-mediated host metabolic reprogramming |
| url | https://journals.asm.org/doi/10.1128/msystems.00197-23 |
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