Unveiling Prasinovirus diversity and host specificity through targeted enrichment in the South China Sea.

IF 5.1 Q1 ECOLOGY ISME communications Pub Date : 2024-08-29 eCollection Date: 2024-01-01 DOI:10.1093/ismeco/ycae109
Julie Thomy, Frederic Sanchez, Camille Prioux, Sheree Yau, Yangbing Xu, Julian Mak, Ruixian Sun, Gwenael Piganeau, Charmaine C M Yung
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Abstract

Unicellular green picophytoplankton from the Mamiellales order are pervasive in marine ecosystems and susceptible to infections by prasinoviruses, large double-stranded DNA viruses within the Nucleocytoviricota phylum. We developed a double-stranded DNA virus enrichment and shotgun sequencing method, and successfully assembled 80 prasinovirus genomes from 43 samples in the South China Sea. Our research delivered the first direct estimation of 94% accuracy in correlating genome similarity to host range. Stirkingly, our analyses uncovered unexpected host-switching across diverse algal lineages, challenging the existing paradigms of host-virus co-speciation and revealing the dynamic nature of viral evolution. We also detected six instances of horizontal gene transfer between prasinoviruses and their hosts, including a novel alternative oxidase. Additionally, diversifying selection on a major capsid protein suggests an ongoing co-evolutionary arms race. These insights not only expand our understanding of prasinovirus genomic diversity but also highlight the intricate evolutionary mechanisms driving their ecological success and shaping broader virus-host interactions in marine environments.

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通过在中国南海进行定向富集,揭示 Prasinovirus 的多样性和宿主特异性。
单细胞绿色浮游动物(Mamiellales)普遍存在于海洋生态系统中,易受prasinoviruses(核细胞病毒门中的大型双链DNA病毒)感染。我们开发了一种双链DNA病毒富集和霰弹枪测序方法,并从中国南海的43个样本中成功组装了80个prasinovirus基因组。我们的研究首次直接估算出基因组相似性与宿主范围相关性的准确率为 94%。令人震惊的是,我们的分析发现了不同藻系之间意想不到的宿主转换,挑战了现有的宿主-病毒共种模式,揭示了病毒进化的动态本质。我们还发现了六种朊病毒与其宿主之间的水平基因转移,其中包括一种新型替代氧化酶。此外,对一种主要囊膜蛋白的多样化选择也表明了一场持续的共同进化军备竞赛。这些发现不仅拓展了我们对朊病毒基因组多样性的理解,而且还凸显了驱动其生态成功的复杂进化机制,并影响了海洋环境中更广泛的病毒-宿主相互作用。
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