Viruses directly affect the most important biological processes in the ocean via their regulation of prokaryotic and eukaryotic populations. Marine sponges form stable symbiotic partnerships with a wide diversity of microorganisms and this high symbiont complexity makes them an ideal model for studying viral ecology. Here, we used morphological and molecular approaches to illuminate the diversity and function of viruses inhabiting nine sponge species from the Great Barrier Reef and seven from the Red Sea. Viromic sequencing revealed host-specific and site-specific patterns in the viral assemblages, with all sponge species dominated by the bacteriophage order Caudovirales but also containing variable representation from the nucleocytoplasmic large DNA virus families Mimiviridae, Marseilleviridae, Phycodnaviridae, Ascoviridae, Iridoviridae, Asfarviridae and Poxviridae. Whilst core viral functions related to replication, infection and structure were largely consistent across the sponge viromes, functional profiles varied significantly between species and sites largely due to differential representation of putative auxiliary metabolic genes (AMGs) and accessory genes, including those associated with herbicide resistance, heavy metal resistance and nylon degradation. Furthermore, putative AMGs varied with the composition and abundance of the sponge-associated microbiome. For instance, genes associated with antimicrobial activity were enriched in low microbial abundance sponges, genes associated with nitrogen metabolism were enriched in high microbial abundance sponges and genes related to cellulose biosynthesis were enriched in species that host photosynthetic symbionts. Our results highlight the diverse functional roles that viruses can play in marine sponges and are consistent with our current understanding of sponge ecology. Differential representation of putative viral AMGs and accessory genes across sponge species illustrate the diverse suite of beneficial roles viruses can play in the functional ecology of these complex reef holobionts.

中文翻译：

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多孔动物门的病毒生态基因组学


病毒通过对原核和真核生物种群的调节，直接影响海洋中最重要的生物过程。海洋海绵与多种微生物形成稳定的共生伙伴关系，这种高度共生复杂性使它们成为研究病毒生态学的理想模型。在这里，我们使用形态学和分子方法来阐明居住在大堡礁九种海绵和红海七种海绵中的病毒的多样性和功能。病毒测序揭示了病毒组合中的宿主特异性和位点特异性模式，所有海绵物种均以噬菌体目 Caudovirales 为主，但也包含核胞质大 DNA 病毒科 Mimiviridae、Marseilleviridae、Phycodnaviridae、Ascoviridae、Iridoviridae、Asfarviridae 和痘病毒科。虽然海绵病毒组中与复制、感染和结构相关的核心病毒功能在很大程度上是一致的，但功能谱在物种和位点之间存在显着差异，这主要是由于假定的辅助代谢基因（AMG）和辅助基因的差异表达，包括与除草剂抗性相关的基因、耐重金属和尼龙降解。此外，假定的 AMG 随海绵相关微生物组的组成和丰度而变化。例如，与抗菌活性相关的基因在低微生物丰度海绵中富集，与氮代谢相关的基因在高微生物丰度海绵中富集，与纤维素生物合成相关的基因在拥有光合共生体的物种中富集。 我们的研究结果强调了病毒在海绵中发挥的多种功能作用，并且与我们目前对海绵生态学的理解是一致的。假定的病毒 AMG 和海绵物种的辅助基因的差异表达说明了病毒在这些复杂的珊瑚礁全生物的功能生态中可以发挥的多种有益作用。