Marcelle L Johnson, Dieke Boezen, Alexey A Grum-Grzhimaylo, René A A van der Vlugt, J Arjan G M de Visser, Mark P Zwart
{"title":"分开生活在一起:病毒多部基因组组织的成本和收益的定量观点。","authors":"Marcelle L Johnson, Dieke Boezen, Alexey A Grum-Grzhimaylo, René A A van der Vlugt, J Arjan G M de Visser, Mark P Zwart","doi":"10.3390/v17091275","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Multipartite viruses individually package their multiple genome segments into virus particles, necessitating the transmission of multiple virus particles for effective viral spread. This dependence poses a cost in the form of reduced transmission compared to monopartite viruses, which only have a single genome segment. The notable cost of a multipartite genome organization has spurred debate on why multipartite viruses are so common among plant viruses, including a search for benefits associated with this organizational form.</p><p><strong>Methods: </strong>We investigated the costs and benefits of multipartite viruses with three approaches. First, we reanalyzed dose-response data to measure the cost of multipartition to between-host transmission for multipartite viruses. Second, we developed a simulation model to explore when the sharing of viral gene products between cells is beneficial. Third, we tested whether multipartite viruses have a broad host range by estimating the host range for plant viruses using metagenomics data.</p><p><strong>Results: </strong>We find that the observed cost to transmission exceeds theoretical predictions. We predict that a virus gene-product-sharing strategy only confers benefits under limited conditions, suggesting that this strategy may not be common. Our results suggest that multipartite and segmented viruses have broader host ranges than monopartite viruses.</p><p><strong>Conclusions: </strong>Our analyses also suggest there is limited evidence for the costs and benefits of a multipartite organization, and we argue that the diversity of multipartite virus-host systems demands pluralistic explanatory frameworks.</p>","PeriodicalId":49328,"journal":{"name":"Viruses-Basel","volume":"17 9","pages":""},"PeriodicalIF":3.5000,"publicationDate":"2025-09-20","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12474326/pdf/","citationCount":"0","resultStr":"{\"title\":\"Living Together Apart: Quantitative Perspectives on the Costs and Benefits of a Multipartite Genome Organization in Viruses.\",\"authors\":\"Marcelle L Johnson, Dieke Boezen, Alexey A Grum-Grzhimaylo, René A A van der Vlugt, J Arjan G M de Visser, Mark P Zwart\",\"doi\":\"10.3390/v17091275\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><strong>Background: </strong>Multipartite viruses individually package their multiple genome segments into virus particles, necessitating the transmission of multiple virus particles for effective viral spread. This dependence poses a cost in the form of reduced transmission compared to monopartite viruses, which only have a single genome segment. The notable cost of a multipartite genome organization has spurred debate on why multipartite viruses are so common among plant viruses, including a search for benefits associated with this organizational form.</p><p><strong>Methods: </strong>We investigated the costs and benefits of multipartite viruses with three approaches. First, we reanalyzed dose-response data to measure the cost of multipartition to between-host transmission for multipartite viruses. Second, we developed a simulation model to explore when the sharing of viral gene products between cells is beneficial. Third, we tested whether multipartite viruses have a broad host range by estimating the host range for plant viruses using metagenomics data.</p><p><strong>Results: </strong>We find that the observed cost to transmission exceeds theoretical predictions. We predict that a virus gene-product-sharing strategy only confers benefits under limited conditions, suggesting that this strategy may not be common. Our results suggest that multipartite and segmented viruses have broader host ranges than monopartite viruses.</p><p><strong>Conclusions: </strong>Our analyses also suggest there is limited evidence for the costs and benefits of a multipartite organization, and we argue that the diversity of multipartite virus-host systems demands pluralistic explanatory frameworks.</p>\",\"PeriodicalId\":49328,\"journal\":{\"name\":\"Viruses-Basel\",\"volume\":\"17 9\",\"pages\":\"\"},\"PeriodicalIF\":3.5000,\"publicationDate\":\"2025-09-20\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC12474326/pdf/\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Viruses-Basel\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.3390/v17091275\",\"RegionNum\":3,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q2\",\"JCRName\":\"VIROLOGY\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Viruses-Basel","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.3390/v17091275","RegionNum":3,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q2","JCRName":"VIROLOGY","Score":null,"Total":0}
Living Together Apart: Quantitative Perspectives on the Costs and Benefits of a Multipartite Genome Organization in Viruses.
Background: Multipartite viruses individually package their multiple genome segments into virus particles, necessitating the transmission of multiple virus particles for effective viral spread. This dependence poses a cost in the form of reduced transmission compared to monopartite viruses, which only have a single genome segment. The notable cost of a multipartite genome organization has spurred debate on why multipartite viruses are so common among plant viruses, including a search for benefits associated with this organizational form.
Methods: We investigated the costs and benefits of multipartite viruses with three approaches. First, we reanalyzed dose-response data to measure the cost of multipartition to between-host transmission for multipartite viruses. Second, we developed a simulation model to explore when the sharing of viral gene products between cells is beneficial. Third, we tested whether multipartite viruses have a broad host range by estimating the host range for plant viruses using metagenomics data.
Results: We find that the observed cost to transmission exceeds theoretical predictions. We predict that a virus gene-product-sharing strategy only confers benefits under limited conditions, suggesting that this strategy may not be common. Our results suggest that multipartite and segmented viruses have broader host ranges than monopartite viruses.
Conclusions: Our analyses also suggest there is limited evidence for the costs and benefits of a multipartite organization, and we argue that the diversity of multipartite virus-host systems demands pluralistic explanatory frameworks.
期刊介绍:
Viruses (ISSN 1999-4915) is an open access journal which provides an advanced forum for studies of viruses. It publishes reviews, regular research papers, communications, conference reports and short notes. Our aim is to encourage scientists to publish their experimental and theoretical results in as much detail as possible. There is no restriction on the length of the papers. The full experimental details must be provided so that the results can be reproduced. We also encourage the publication of timely reviews and commentaries on topics of interest to the virology community and feature highlights from the virology literature in the ''News and Views'' section. Electronic files or software regarding the full details of the calculation and experimental procedure, if unable to be published in a normal way, can be deposited as supplementary material.