Phages as metabolic switches in plant-associated microbiomes: implications for climate-smart agriculture

Bacteriophages constitute a regulatory layer in plant-associated microbiomes that has been systematically under-characterized relative to their ecological importance. This review advances the hypothesis that phages function as metabolic switches, alternating between lytic nutrient release and lysogenic host-fitness enhancement to govern the microbial metabolic states that determine nutrient cycling, stress responses, and microbiome stability in the rhizosphere and phyllosphere. During lytic infection, phage-driven cell lysis releases dissolved organic carbon, ammonium, and phosphate through the viral shunt, redistributing microbial biomass into forms directly accessible to plant roots and surviving microbial taxa. Lysogenic integration, by contrast, delivers prophage-encoded auxiliary metabolic genes that reprogram bacterial hosts with enhanced metabolic capacity across multiple generations without immediate cell death. Environmental stressors, include drought, salinity, temperature extremes, heavy metal contamination, and pathogen pressure remodel root exudation profiles, alter microbial metabolic bottlenecks, and shift phage life-cycle decisions through quorum-sensing-responsive and SOS-dependent switching mechanisms. These phage-mediated processes have cascading consequences for plant-relevant outcomes including nutrient uptake efficiency, oxidative stress management, phytohormone signaling, and growth-defense trade-offs mediated by plant growth-promoting rhizobacteria. By integrating mechanistic evidence across abiotic and biotic stress contexts, this review proposes a phage-microbe-plant metabolic axis as a unifying framework for understanding how soil virome dynamics translate into plant physiological outcomes. Practical implications for engineering phage-informed microbiomes and developing climate-resilient agricultural systems are evaluated alongside ecological risks, knowledge gaps, and priorities for field validation, virome mapping, and predictive modeling that must be addressed before phage-based interventions can be reliably deployed in crop production.