Virus-mediated prokaryotic community adaptation dynamics under thermal stress in municipal organic solid waste microbiomes

Temperature influences microbial metabolic activity, which is crucial for biotechnological processes and bioproducts stabilization. However, temperature-driven responses of complex viruses and prokaryotic communities, and the modulatory role of viruses in prokaryotic community within environmental biotechnology systems, remain poorly understood. We developed a continuous thermal stress system with temperature gradients and high-resolution temporal sampling of metagenomics and metatranscriptomics, using municipal organic solid waste as a biological model. An optimized meta-omics pipeline integrating genomic potential and activity was applied to investigate the adaptive dynamics of complex prokaryotic and viral communities. Continuous thermal stress triggered stress responses in paired virus-hosts within the system. Thermal stress exerted distinct effects on temperate and virulent viruses. Viruses formed quasi-symbiotic alliances with their hosts to withstand thermal stress by integrating protein folding genes, stress response, and metabolic function genes, shaping host adaptability under thermal pressure. Equipped with multiple defense and counter-defense systems, viruses accelerated the accumulation of beneficial mutations under thermal stress, enabling them to escape host immunity and intensify competition with prokaryotic communities. This study demonstrates how viruses accelerated both the restructuring and adaptive responses of prokaryotic communities under thermal stress, advancing our understanding of phage-based therapeutic strategies in temperature-variable engineering applications.