Soil viruses are underexplored players in ecosystem carbon processing

Abstract

Rapidly thawing permafrost harbors ~30-50% of global soil carbon, and the fate of this carbon remains unknown. Microorganisms will play a central role in its fate, and their viruses could modulate that impact via induced mortality and metabolic controls. Because of the challenges of recovering viruses from soils, little is known about soil viruses or their role(s) in microbial biogeochemical cycling. Here, we describe 53 viral populations (vOTUs) recovered from seven quantitatively-derived (i.e. not multiple-displacement-amplified) viral-particle metagenomes (viromes) along a permafrost thaw gradient. Only 15% of these vOTUs had genetic similarity to publicly available viruses in the RefSeq database, and ~30% of the genes could be annotated, supporting the concept of soils as reservoirs of substantial undescribed viral genetic diversity. The vOTUs exhibited distinct ecology, with dramatically different distributions along the thaw gradient habitats, and a shift from soil-virus-like assemblages in the dry palsas to aquatic-virus-like in the inundated fen. Seventeen vOTUs were linked to microbial hosts (in silico), implicating viruses in infecting abundant microbial lineages from Acidobacteria, Verrucomicrobia, and Deltaproteoacteria, including those encoding key biogeochemical functions such as organic matter degradation. Thirty-one auxiliary metabolic genes (AMGs) were identified, and suggested viral-mediated modulation of central carbon metabolism, soil organic matter degradation, polysaccharide-binding, and regulation of sporulation. Together these findings suggest that these soil viruses have distinct ecology, impact host-mediated biogeochemistry, and likely impact ecosystem function in the rapidly changing Arctic.