Okazaki Yusuke, Nishikawa Yohei, Wagatsuma Ryota, Takeyama Haruko, Nakano Shin-Ichi
Institute for Chemical Research, Kyoto University, Gokasho, Uji, Kyoto 611-0011, Japan.
Computational Bio Big-Data Open Innovation Laboratory, AIST-Waseda University, 3-4-1 Okubo, Shinjuku-ku, Tokyo 169-0072, Japan.
ISME Commun. 2025 May 21;5(1):ycaf086. doi: 10.1093/ismeco/ycaf086. eCollection 2025 Jan.
Characterizing virus-host pairs and the infection state of individual cells is the major technical challenge in microbial ecology. We addressed these challenges using state-of-the-art single-cell genome technology (SAG-gel) combined with extensive metagenomic datasets targeting the bacterial and viral communities in Lake Biwa. From two water layers and two seasons, we obtained 862 single-cell amplified genomes (SAGs), including 176 viral (double-stranded DNA phage) contigs, which identified novel virus-host pairs involving dominant freshwater lineages. The viral infection rate, estimated by mapping the individual SAG's raw reads to viral contigs, showed little variation among samples (12.1%-18.1%) but significant variation in host taxonomy (4.2%-65.3%), with copiotrophs showing higher values than oligotrophs. The high infection rates of copiotrophs were attributed to collective infection by diverse viruses, suggesting weak density-dependent virus-host selection, presumably due to their nonpersistent interactions with viruses resulting from fluctuating abundance. In contrast, the low infection rates of oligotrophs supported the idea that their codominance with viruses is achieved by genomic microdiversification, which diversifies the virus-host specificity, sustained by their large population size and persistent density-dependent fluctuating selection. Notably, we discovered viruses infecting CL500-11, the dominant bacterioplankton lineage in deep freshwater lakes worldwide. These viruses showed extremely high read coverages in cellular and virion metagenomes but were detected in <1% of host cells, suggesting a low infection rate and high burst size. Overall, we revealed highly diverse virus-host interactions within and between host lineages that were overlooked at the metagenomic resolution.
表征病毒-宿主对以及单个细胞的感染状态是微生物生态学中的主要技术挑战。我们利用最先进的单细胞基因组技术（SAG-gel）并结合针对琵琶湖细菌和病毒群落的大量宏基因组数据集来应对这些挑战。从两个水层和两个季节中，我们获得了862个单细胞扩增基因组（SAGs），包括176个病毒（双链DNA噬菌体）重叠群，这些重叠群鉴定出了涉及优势淡水谱系的新型病毒-宿主对。通过将单个SAG的原始读数映射到病毒重叠群来估计的病毒感染率在样本间变化不大（12.1%-18.1%），但在宿主分类学上有显著变化（4.2%-65.3%），富营养菌的值高于贫营养菌。富营养菌的高感染率归因于多种病毒的集体感染，这表明密度依赖性病毒-宿主选择较弱，推测是由于它们与因丰度波动而产生的病毒的非持久性相互作用。相比之下，贫营养菌的低感染率支持了这样一种观点，即它们与病毒的共优势是通过基因组微多样化实现的，这种微多样化使病毒-宿主特异性多样化，并由其庞大的种群规模和持续的密度依赖性波动选择维持。值得注意的是,我们发现了感染CL500-11的病毒，CL500-11是全球深层淡水湖泊中占主导地位的浮游细菌谱系。这些病毒在细胞和病毒体宏基因组中显示出极高的读数覆盖率，但在不到1%的宿主细胞中被检测到，这表明感染率低且爆发大小高。总体而言，我们揭示了宿主谱系内部和之间高度多样的病毒-宿主相互作用，这些相互作用在宏基因组分辨率下被忽视了。
