The microbiomes in macroalgal holobionts play vital roles in regulating macroalgal growth and ocean carbon cycling. However, the virospheres in macroalgal holobionts remain largely underexplored, representing a critical knowledge gap. Here we unveil that the holobiont of kelp (Saccharina japonica) harbors highly specific and unique epiphytic/endophytic viral species, with novelty (99.7% unknown) surpassing even extreme marine habitats (e.g., deep-sea and hadal zones), indicating that macroalgal virospheres, despite being closest to us, are among the least understood. These viruses potentially maintain microbiome equilibrium critical for kelp health via lytic-lysogenic infections and the expression of folate biosynthesis genes. In-situ kelp mesocosm cultivation and metagenomic mining revealed that kelp holobiont profoundly reshaped surrounding seawater and sediment virus-prokaryote pairings through changing surrounding environmental conditions and virus-host migrations. Some kelp epiphytic viruses could even infect sediment autochthonous bacteria after deposition. Moreover, the presence of ample viral auxiliary metabolic genes for kelp polysaccharide (e.g., laminarin) degradation underscores the underappreciated viral metabolic influence on macroalgal carbon cycling. This study provides key insights into understanding the previously overlooked ecological significance of viruses within macroalgal holobionts and the macroalgae-prokaryotes-virus tripartite relationship.

中文翻译：

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巨藻病毒圈有助于宿主-微生物组平衡调节并影响周围海洋环境中的原核生物

巨藻全生物中的微生物组在调节巨藻生长和海洋碳循环中发挥着至关重要的作用。然而，巨藻全生物中的病毒圈在很大程度上仍未得到充分探索，代表了一个关键的知识差距。在这里，我们揭示了海带（Saccharina japonica）的全生物体拥有高度特异性和独特的附生/内生病毒物种，其新颖性（99.7％未知）甚至超越了极端海洋栖息地（例如深海和深渊带），这表明大型藻类病毒圈尽管离我们最近，但却是最不被理解的。这些病毒可能通过溶菌感染和叶酸生物合成基因的表达来维持对海带健康至关重要的微生物组平衡。原位海带中生态培养和宏基因组挖掘表明，海带全生物通过改变周围环境条件和病毒-宿主迁移，深刻重塑了周围海水和沉积物的病毒-原核生物配对。一些海带附生病毒沉积后甚至可以感染沉积物的原生细菌。此外，大量用于海带多糖（例如昆布多糖）降解的病毒辅助代谢基因的存在强调了病毒代谢对巨藻碳循环的影响未被充分认识。这项研究为理解以前被忽视的大型藻类全生物中病毒的生态意义以及大型藻类-原核生物-病毒三方关系提供了重要的见解。