Soil Protists Consume Viruses to Drive Microbial Nutrient Cycling: Overlooked Trophic Pathways in Soil Food Web

Abstract

Soil viruses are traditional top-down regulators that redistribute organic matter through host lysis and the viral shunt, implicitly positioning them as terminal sinks rather than active trophic components. Here, we show, for the first time, that soil viruses can also be direct prey for protists, establishing an overlooked pathway for the transfer of viral-derived nutrients and energy within soil food webs. In controlled cocultures, the ciliate Tetrahymena pyriformis actively ingested the soil bacteriophage HRZ04p, with viral abundance declining by 0.66-log within 24 h at a virus-to-protist ratio of 5:1. Under high viral availability (104:1), viral consumption enhanced protist population growth by 2.24-fold relative to virus-free controls. Viral grazing altered nutrient dynamics, characterized by ammonium peaking at 1,206 μg L–1 (a 92% increase compared with protists alone) and coordinated shifts in nitrogen-metabolizing enzymes. Untargeted metabolomics revealed extensive metabolic reprogramming, with amino acid catabolic pathways upregulated. In contrast, amino acid biosynthesis and aminoacyl-tRNA biosynthesis were simultaneously activated, reflecting recycling of viral-derived substrates into new protein synthesis. These findings confirm the existence of a soil “viral consumption” pathway, reposition viruses as active nodes within microbial food webs, and provide a mechanistic and conceptual foundation for incorporating virus-mediated nutrient fluxes into soil biogeochemical models.