Bulzu Paul-Adrian, Henriques Vieira Helena, Ghai Rohit
Department of Aquatic Microbial Ecology, Institute of Hydrobiology, Biology Centre of the Czech Academy of Sciences, České Budějovice, Czech Republic.
Microbiome. 2025 Jul 1;13(1):154. doi: 10.1186/s40168-025-02148-0.
Polinton-like viruses (PLVs) are diverse eukaryotic DNA viral elements (14-40 kb) that often undergo significant expansion within protist genomes through repeated insertion events. Emerging evidence indicates they function as antiviral defense systems in protists, reducing the progeny yield of their infecting giant viruses (phylum Nucleocytoviricota) and influencing the population dynamics and evolution of both viruses and their hosts. While many PLVs have been identified within the genomes of sequenced protists, most were recovered from metagenomic data. Even with the large number of PLVs identified from metagenomic data, their host-virus linkages remain unknown owing to the scarcity of ecologically relevant protist genomes. Additionally, the extent of PLV diversification within abundant freshwater taxa remains undetermined. In order to tackle these questions, high-quality genomes of abundant and representative taxa that bridge genomic and metagenomic PLVs are necessary. In this regard, cryptophytes, which are among the most widely distributed, abundant organisms in freshwaters and have remained largely out of bounds of genomic and metagenomic approaches, are ideal candidates for investigating the diversification of such viral elements both in cellular and environmental context.
We leveraged long-read sequencing to recover large (200-600 Mb), high-quality, and highly repetitive (> 60%) genomes of representative freshwater and marine photosynthetic cryptophytes. We uncovered over a thousand complete PLVs within these genomes, revealing vast lineage-specific expansions, particularly in the common freshwater cryptophyte Rhodomonas lacustris. By combining deep sequence homology annotation with biological network analyses, we discern well-defined PLV groups defined by characteristic gene-sharing patterns and the use of distinct strategies for replication and integration within host genomes. Finally, the PLVs recovered from these cryptophyte genomes also allow us to assign host-virus linkages in environmental sequencing data.
Our findings provide a primer for understanding the evolutionary history, gene content, modes of replication and infection strategies of cryptophyte PLVs, with special emphasis on their expansion as endogenous viral elements (EVEs) in freshwater bloom-forming R. lacustris. Video Abstract.
类波林顿病毒（PLVs）是多样的真核生物DNA病毒元件（14 - 40 kb），常通过重复插入事件在原生生物基因组内发生显著扩增。新出现的证据表明，它们在原生生物中作为抗病毒防御系统发挥作用，降低感染它们的巨型病毒（核质巨DNA病毒门）的子代产量，并影响病毒及其宿主的种群动态和进化。虽然在已测序原生生物的基因组中已鉴定出许多PLVs，但大多数是从宏基因组数据中获得的。即使从宏基因组数据中鉴定出大量PLVs，由于缺乏与生态相关的原生生物基因组，它们的宿主 - 病毒联系仍然未知。此外，丰富的淡水类群中PLV多样化的程度仍未确定。为了解决这些问题，需要有丰富且具代表性的类群的高质量基因组，以连接基因组和宏基因组中的PLVs。在这方面，隐藻是淡水中分布最广、数量最多的生物之一，并且在很大程度上仍未被基因组学和宏基因组学方法所触及，是在细胞和环境背景下研究此类病毒元件多样化的理想候选对象。
我们利用长读长测序技术获得了具有代表性的淡水和海洋光合隐藻的大型（200 - 600 Mb）、高质量且高度重复（> 60%）的基因组。我们在这些基因组中发现了一千多个完整的PLVs，揭示了巨大的谱系特异性扩增，特别是在常见的淡水隐藻湖生红胞藻中。通过将深度序列同源性注释与生物网络分析相结合，我们识别出了由特征性基因共享模式以及在宿主基因组内复制和整合所使用的不同策略所定义的明确的PLV组。最后，从这些隐藻基因组中获得的PLVs也使我们能够在环境测序数据中确定宿主 - 病毒联系。
我们的研究结果为理解隐藻PLVs的进化历史、基因内容、复制模式和感染策略提供了一个入门指南，特别强调了它们作为淡水水华形成的湖生红胞藻中的内源性病毒元件（EVEs）的扩增。视频摘要。
