Metatranscriptomic reconstruction reveals RNA viruses with the potential to shape carbon cycling in soil

Abstract

Viruses impact nearly all organisms on Earth, with ripples of influence in agriculture, health, and biogeochemical processes. However, very little is known about RNA viruses in an environmental context, and even less is known about their diversity and ecology in soil, 1 of the most complex microbial systems. Here, we assembled 48 individual metatranscriptomes from 4 habitats within a planted soil sampled over a 22-d time series: Rhizosphere alone, detritosphere alone, rhizosphere with added root detritus, and unamended soil (4 time points and 3 biological replicates). We resolved the RNA viral community, uncovering a high diversity of viral sequences. We also investigated possible host organisms by analyzing metatranscriptome marker genes. Based on viral phylogeny, much of the diversity was Narnaviridae that may parasitize fungi or Leviviridae, which may infect Proteobacteria. Both host and viral communities appear to be highly dynamic, and rapidly diverged depending on experimental conditions. The viral and host communities were structured based on the presence of root litter. Clear temporal dynamics by Leviviridae and their hosts indicated that viruses were replicating. With this time-resolved analysis, we show that RNA viruses are diverse, abundant, and active in soil. When viral infection causes host cell death, it may mobilize cell carbon in a process that may represent an overlooked component of soil carbon cycling.

Keywords: metatranscriptome; phage; rhizosphere; soil; virus.

Fig. 1.

Phylogenetic trees representing clades of RNA viruses (based on RdRp) identified in our California annual grassland experimental soil. Within each tree, the RdRp sequences we identified are colored purple and previously described sequences are in pink. Trees are all midpoint rooted. Trees with predicted fungal infecting clades are presented in SI Appendix, Fig. S1.

Fig. 2.

Nonmetric multidimensional scaling ordination of soil eukaryotic communities in response to 4 soil resource treatments, based on coverage of the Cox1 gene (A. fatua sequences removed) (A), and ordination of eukaryotic RNA viral communities with coverage calculated at the scaffold level (B).

Fig. 3.

Nonmetric multidimensional scaling ordination of the Leviviridae community identified in an annual grassland soil exposed to 4 resource treatments, colored by time (A) and treatment (B).