Underexplored Territory: Viromics Reveals the Diversity, Spatial Heterogeneity and Potential Ecosystem Impacts of RNA Viruses in Soils

Abstract:

Viruses play a crucial and underexplored role in soil microbial ecosystems, but soil viral ecology has focused almost exclusively on DNA bacteriophages. Despite their significant impact on public health and food security, the role of RNA viruses in soil ecosystems has largely been overlooked. Here, we report the first direct analysis of soil RNA viral communities. Virus-like-particles were purified from peatland soil, grassland soil under intensive and extensive management and coastal sediment along an altitudinal primary productivity gradient. Total RNA was extracted from triplicate samples and sequenced using an Illumina HiSeq 4000. We used HMMER to identify 3,471 viral RdRp containing sequences, of which 1654 were unclassified by BLAST. Sampling sites showed low similarity in viral community composition but with >10-fold more contigs shared between grassland sites than with peatland or coastal sites. The lack of a clear core terrestrial RNA virome in our study suggests extensive unexplored soil RNA viral diversity. Phylogenetic analysis predicted that 12% of identified viral contigs belonged to the prokaryote-infecting Leviviridae family, contrasting with a previous study where RNA viral sequences recovered from bulk soil metatranscriptomes were dominated by this family. This suggests that a combination of the two protocols, bulk virus-like particle extraction followed by RNA sequencing and bulk soil metatranscriptomics, may reveal more viral diversity than when used individually. Our study represents an important step towards the characterisation of soil viral communities and the intricate interactions with their hosts at multiple trophic levels, which will provide a more holistic view of the biology of economically and ecologically important soils.