While decomposition of organic matter by bacteria plays a major role in nutrient cycling in terrestrial ecosystems, the significance of viruses remains poorly understood. Here we combined metagenomics and metatranscriptomics with temporal sampling to study the significance of mesophilic and thermophilic bacteria and their viruses on nutrient cycling during industrial-scale hyperthermophilic composting (HTC). Our results show that virus-bacteria density dynamics and activity are tightly coupled, where viruses specific to mesophilic and thermophilic bacteria track their host densities, triggering microbial community succession via top-down control during HTC. Moreover, viruses specific to mesophilic bacteria encoded and expressed several auxiliary metabolic genes (AMGs) linked to carbon cycling, impacting nutrient turnover alongside bacteria. Nutrient turnover correlated positively with virus–host ratio, indicative of a positive relationship between ecosystem functioning, viral abundances, and viral activity. These effects were predominantly driven by DNA viruses as most detected RNA viruses were associated with eukaryotes and not associated with nutrient cycling during the thermophilic phase of composting. Our findings suggest that DNA viruses could drive nutrient cycling during HTC by recycling bacterial biomass through cell lysis and by expressing key AMGs. Viruses could hence potentially be used as indicators of microbial ecosystem functioning to optimize productivity of biotechnological and agricultural systems.

虽然细菌分解有机物在陆地生态系统的养分循环中发挥着重要作用，但病毒的重要性仍然知之甚少。在这里，我们将宏基因组学和宏转录组学与时间采样相结合，研究嗜温和嗜热细菌及其病毒对工业规模超高温堆肥（HTC）期间营养循环的重要性。我们的结果表明，病毒-细菌密度动态和活性紧密耦合，其中嗜温和嗜热细菌特有的病毒追踪其宿主密度，在 HTC 期间通过自上而下的控制触发微生物群落演替。此外，嗜温细菌特有的病毒编码并表达了几种与碳循环相关的辅助代谢基因（AMG），与细菌一起影响营养物质的周转。养分周转与病毒-宿主比率呈正相关，表明生态系统功能、病毒丰度和病毒活性之间存在正相关关系。这些影响主要由 DNA 病毒驱动，因为大多数检测到的 RNA 病毒与真核生物有关，与堆肥高温阶段的营养循环无关。我们的研究结果表明，DNA 病毒可以通过细胞裂解回收细菌生物量并表达关键的 AMG，从而在 HTC 期间驱动营养循环。因此，病毒有可能被用作微生物生态系统功能的指标，以优化生物技术和农业系统的生产力。