Giant viruses significantly regulate the ecological dynamics of diverse ecosystems. Although metagenomics has expanded our understanding of their diversity and ecological roles played in marine environments, little is known about giant viruses of freshwater ecosystems. Most previous studies have employed short-read sequencing and therefore resulted in fragmented genomes, hampering accurate assessment of genetic diversity. We sought to bridge this knowledge gap and overcome previous technical limitations. We subjected spatiotemporal (2 depths × 12 months) samples from Lake Biwa to metagenome-assembled genome reconstruction enhanced by long-read metagenomics. This yielded 293 giant virus metagenome-assembled genomes. Of these, 285 included previously unknown species in five orders of nucleocytoviruses and the first representatives of freshwater mirusviruses, which exhibited marked divergence from marine-derived lineages. The good performance of our long-read metagenomic assembly was demonstrated by the detection of 42 (14.3%) genomes composed of single contigs with completeness values >90%. Giant viruses were partitioned across water depths, with most species specific to either the sunlit epilimnion or the dark hypolimnion. Epilimnion-specific members tended to be transient and exhibit short and intense abundance peaks, in line with the fact that they regulate the surface algal blooms. During the spring bloom, mirusviruses and members of three nucleocytovirus families were among the most abundant viruses. In contrast, hypolimnion-specific ones including a mirusvirus genome were typically more persistent in the hypolimnion throughout the water-stratified period, suggesting that they infect hosts specific to the hypolimnion and play previously unexplored ecological roles in dark water microbial ecosystems.

中文翻译：

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深淡水湖中巨型病毒的时空动态揭示了一个独特的黑水群落


巨型病毒显著调节不同生态系统的生态动态。尽管宏基因组学扩大了我们对它们的多样性和在海洋环境中发挥的生态作用的理解，但人们对淡水生态系统中的巨型病毒知之甚少。以前的大多数研究都采用了短读长测序，因此导致基因组碎片化，阻碍了对遗传多样性的准确评估。我们试图弥合这一知识差距并克服以前的技术限制。我们将来自琵琶湖的时空 （2 个深度× 12 个月） 样本进行了长读长宏基因组学增强的宏基因组组装基因组重建。这产生了 293 个巨型病毒宏基因组组装的基因组。其中，285 个包括核细胞病毒 5 个目中以前未知的物种和淡水 mirusvirus 的第一个代表，它们表现出与海洋衍生谱系的明显差异。通过检测到 42 个 （14.3%） 由具有完整性值 >90% 的单个重叠群组成的基因组，证明了我们的长读长宏基因组组装的良好性能。巨型病毒分布在水深处，大多数物种特有于阳光照射的表层或深色的下层。Epilimnion 特异性成员往往是瞬态的，并表现出短暂而强烈的丰度峰值，这与它们调节表面藻华的事实一致。在春花期间，mirusviruses 和 3 个核细胞病毒家族的成员是数量最多的病毒之一。 相比之下，包括 mirusvirus 基因组在内的 hypolimnion 特异性通常在整个水分层期间在 hypolimnion 中更持久，这表明它们感染了 hypolimnion 特有的宿主，并在暗水微生物生态系统中发挥着以前未探索的生态作用。