Eco-environment and Resource Efficiency Research Laboratory, School of Environment and Energy, Peking University Shenzhen Graduate School, Shenzhen, 518055, PR China.
Environmental Microbiome and Innovative Genomics Laboratory, College of Environmental Sciences and Engineering, Peking University, Beijing, 100871, PR China.
ISME J. 2023 Oct;17(10):1719-1732. doi: 10.1038/s41396-023-01481-2. Epub 2023 Jul 31.
Bacterial pathogens and viruses are the leading causes of global waterborne diseases. Here, we discovered an interesting natural paradigm of water "self-purification" through virus-pathogen interactions over a 1432 km continuum along the Middle Route of the South-to-North Water Diversion Canal (MR-SNWDC) in China, the largest water transfer project in the world. Due to the extremely low total phosphorus (TP) content (ND-0.02 mg/L) in the MR-SNWDC, the whole canal has experienced long-lasting phosphorus (P) limitation since its operation in 2015. Based on 4443 metagenome-assembled genomes (MAGs) and 40,261 nonredundant viral operational taxonomic units (vOTUs) derived from our recent monitoring campaign, we found that residential viruses experiencing extreme P constraints had to adopt special adaptive strategies by harboring smaller genomes to minimize nucleotide replication, DNA repair, and posttranslational modification costs. With the decreasing P supply downstream, bacterial pathogens showed repressed environmental fitness and growth potential, and a weakened capacity to maintain P acquisition, membrane formation, and ribonucleotide biosynthesis. Consequently, the unique viral predation effects under P limitation, characterized by enhanced viral lytic infections and an increased abundance of ribonucleotide reductase (RNR) genes linked to viral nuclear DNA replication cycles, led to unexpectedly lower health risks from waterborne bacterial pathogens in the downstream water-receiving areas. These findings highlighted the great potential of water self-purification associated with virus-pathogen dynamics for water-quality improvement and sustainable water resource management.
细菌病原体和病毒是全球水传播疾病的主要原因。在这里，我们在中国南水北调中线工程（MR-SNWDC）沿线 1432 公里的连续体上发现了一个有趣的水“自净”自然范例，这是世界上最大的调水工程。由于 MR-SNWDC 中总磷（TP）含量极低（ND-0.02mg/L），自 2015 年工程运行以来，整个运河一直经历着长期的磷（P）限制。基于最近监测活动中获得的 4443 个宏基因组组装基因组（MAG）和 40261 个非冗余病毒分类操作单元（vOTU），我们发现，居住在极端 P 限制下的病毒不得不通过携带更小的基因组来采用特殊的适应策略，以最小化核苷酸复制、DNA 修复和翻译后修饰的成本。随着下游 P 供应的减少，细菌病原体的环境适应性和生长潜力受到抑制，维持磷获取、膜形成和核糖核苷酸生物合成的能力减弱。因此，在 P 限制下，独特的病毒捕食作用表现为增强的病毒裂解感染和与病毒核 DNA 复制周期相关的核糖核苷酸还原酶（RNR）基因的丰度增加，导致下游受水区的水传播细菌病原体的健康风险出人意料地降低。这些发现突出了与病毒-病原体动态相关的水自净在改善水质和可持续水资源管理方面的巨大潜力。
