Fang Yue, Meng Lingjie, Xia Jun, Gotoh Yasuhiro, Hayashi Tetsuya, Nagasaki Keizo, Endo Hisashi, Okazaki Yusuke, Ogata Hiroyuki
Institute for Chemical Research, Kyoto University, Uji, Japan.
Department of Bacteriology, Faculty of Medical Sciences, Kyushu University, Fukuoka, Japan.
mSystems. 2025 Jan 21;10(1):e0116824. doi: 10.1128/msystems.01168-24. Epub 2024 Dec 23.
Giant viruses are crucial for marine ecosystem dynamics because they regulate microeukaryotic community structure, accelerate carbon and nutrient cycles, and drive the evolution of their hosts through co-evolutionary processes. Previously reported long-term observations revealed that these viruses display seasonal fluctuations in abundance. However, the underlying genetic mechanisms driving such dynamics of these viruses remain largely unknown. In this study, we investigated the dynamics of giant viruses using time-series metagenomes from eutrophic coastal seawater samples collected over 20 months. A newly developed computational pipeline generated 1,065 high-quality genomes covering six major giant virus lineages. These genomic data revealed year-round recovery of the viral community structure at the study site and distinct dynamics of viral populations that were classified as persistent ( = 9), seasonal ( = 389), sporadic ( = 318), or others. By profiling the intra-species nucleotide-resolved microdiversity through read mapping, we also identified year-round recovery dynamics at subpopulation level for viruses classified as persistent or seasonal. Our results further indicated that giant viruses with broader niche breadth tended to exhibit higher levels of microdiversity. We argue that greater microdiversity of viruses likely enhances adaptability and thus survival under the virus-host arms race during prolonged interactions with their hosts.IMPORTANCERecent genome-resolved metagenomic surveys have uncovered the vast genomic diversity of giant viruses, which play significant roles in aquatic ecosystems by acting as bloom terminators and influencing biogeochemical cycles. However, the relationship between the ecological dynamics of giant viruses and underlying genetic structures of viral populations remains unresolved. In this study, we performed deep metagenomic sequencing of seawater samples collected across a time-series from a coastal area in Japan. The results revealed a significant positive correlation between microdiversity and temporal persistence of giant virus populations, suggesting that population structure is a crucial factor for adaptation and survival in the interactions with their hosts.
巨型病毒对海洋生态系统动态至关重要，因为它们调节微型真核生物群落结构，加速碳和养分循环，并通过共同进化过程推动宿主的进化。先前报道的长期观测表明，这些病毒的丰度呈现季节性波动。然而，驱动这些病毒这种动态变化的潜在遗传机制在很大程度上仍不为人知。在本研究中，我们使用从富营养化沿海海水样本中收集的长达20个月的时间序列宏基因组来研究巨型病毒的动态变化。一个新开发的计算流程生成了1065个高质量基因组，涵盖六个主要的巨型病毒谱系。这些基因组数据揭示了研究地点病毒群落结构的全年恢复情况，以及被分类为持续存在型（=9）、季节型（=389）、散发型（=318）或其他类型的病毒种群的不同动态变化。通过读取映射分析种内核苷酸分辨率的微多样性，我们还确定了被分类为持续存在型或季节型的病毒在亚种群水平上的全年恢复动态。我们的结果进一步表明，生态位宽度更广的巨型病毒往往表现出更高水平的微多样性。我们认为，病毒更大的微多样性可能增强其适应性，从而在与宿主的长期相互作用中的病毒 - 宿主军备竞赛中生存下来。
重要性
最近基于基因组解析的宏基因组学调查揭示了巨型病毒巨大的基因组多样性，它们通过充当水华终结者和影响生物地球化学循环在水生生态系统中发挥重要作用。然而，巨型病毒的生态动态与病毒种群潜在遗传结构之间的关系仍未得到解决。在本研究中，我们对从日本沿海地区按时间序列收集的海水样本进行了深度宏基因组测序。结果揭示了巨型病毒种群的微多样性与时间持久性之间存在显著正相关，这表明种群结构是它们与宿主相互作用中适应和生存的关键因素。
