Living Together Apart: Quantitative Perspectives on the Costs and Benefits of a Multipartite Genome Organization in Viruses.

IF 3.5 3区 医学 Q2 VIROLOGY
Viruses-Basel Pub Date : 2025-09-20 DOI:10.3390/v17091275
Marcelle L Johnson, Dieke Boezen, Alexey A Grum-Grzhimaylo, René A A van der Vlugt, J Arjan G M de Visser, Mark P Zwart
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Abstract

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.

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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。
背景:多部病毒将其多个基因组片段单独包装成病毒颗粒,需要通过多个病毒颗粒进行有效传播。与只有单一基因组片段的单甲病毒相比,这种依赖性造成了传播减少的代价。多部分基因组组织的显著成本引发了关于为什么多部分病毒在植物病毒中如此普遍的争论,包括寻找与这种组织形式相关的好处。方法:采用三种方法研究多部病毒的成本和收益。首先,我们重新分析了剂量-反应数据,以测量多分区病毒在宿主间传播的成本。其次,我们开发了一个模拟模型来探索细胞间病毒基因产物的共享何时是有益的。第三,我们利用宏基因组学数据估计植物病毒的寄主范围,以测试多部病毒是否具有广泛的寄主范围。结果:我们发现观测到的传输成本超过了理论预测。我们预测,病毒基因-产物共享策略仅在有限条件下提供益处,这表明该策略可能并不常见。我们的研究结果表明,多部病毒和节段病毒比单部病毒具有更广泛的宿主范围。结论:我们的分析还表明,关于多方组织的成本和收益的证据有限,我们认为多方病毒-宿主系统的多样性需要多元的解释框架。
本文章由计算机程序翻译,如有差异,请以英文原文为准。
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来源期刊
Viruses-Basel
Viruses-Basel VIROLOGY-
CiteScore
7.30
自引率
12.80%
发文量
2445
审稿时长
1 months
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.
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