Impact of Soil Moisture on Shaping the DNA and RNA Virome

Due to the recent COVID-19 pandemic, there is increasing interest in understanding environmental reservoirs of viruses and detecting their activities in response to environmental perturbations. Here, we screened a Kansas native prairie soil for DNA and RNA viruses and determined how they responded to soil wetting and drying. We used a multi-omics approach (metagenomics, metatranscriptomics and metaproteomics) to screen for viral sequences and to determine which viruses were active. Activity of the soil DNA virome was assessed by mapping transcripts to DNA viral sequences mined from Kansas native prairie soil metagenomes and public databases (IMG_VR, NCBI virus). Significantly more DNA viral sequences were detected as transcribed (active) in soils dried for 48 h. However, a greater extent of viral activity (more transcriptome reads) were detected in wet soils, suggesting that soil wetting may stimulate the transcriptional activities of a subset of DNA viruses and/or their hosts. Viral genes encoding structural (e.g. tail, capsid) and infection-related (e.g. protease, DNA polymerase) proteins were detected in both Kansas metatranscriptomes and metaproteomes, highlighting that viral infection was an ongoing process in the soils. Several auxiliary metabolic genes (AMGs) were also expressed. Furthermore, we detected a diverse RNA virome in the soil under both wet and dry conditions. The most highly abundant RNA viruses in the soil were Reoviridae; whereas the most diverse RNA viruses were Leviviridae found more abundant in wet soil. Our study is the first to integrate multi-omics information for simultaneous detection of both DNA and RNA viruses in soil and their activity in response to the differences in soil moisture.