Unearthing the Global Soil Microbial-Associated Virome and (u)MAPping the Tectonics of its AlphaFOLD2-Aware Structural Diversity Upon a One Health Framework

Viruses of soil-inhabiting microbes are major drivers of ecosystems but can also mediate diseases to economically important crops or animals and therefore represent a serious burden to global health. Surprisingly, the microbial-associated virus diversity remains speculative. Insofar, and despite the significance of soil microbial lifeforms, no research focusing explicitly on large scale analysis of soil-associated viromes has been carried out making it challenging to mitigate the emergence of soil-associated pathogens. Here,
through extensive metatranscriptomic analysis of retrieved soil genomic data, including rhizosphere, decaying compost and leaf litter, we demonstrate that soil microbes, are a remarkable niche to viruses, constituting one of the most biodiverse hosting ecosystems. Using our novel Modulome approach as a proof-of-concept, we accurately investigate viral proteomic data associated with soil-inhabiting cellular organisms, with a focus on emerging taxonomic lineages. By combining our computational Alphafold2-predicted structural information with Ai-driven statistics based on manifold deep learning for dimension reduction (UMAP), over 250.000 viruses across 20 well-supported RdRp-based hylogenetic lineages were uncovered in diverse soil-inhabiting microbial cryptic hosts, ranging from protists to fungi. Taken together, most speciose taxa were prevalently hosted by Fungi and Chromista kingdoms, thereby enriching our understanding of the uncharted viral diversity and evolution in their soil ecological niche. Finally, our enumeration can enable stakeholders to accurately advocate for better soil health policy while facing global biodiversity crisis and climate change-linked epidemic risks within a more comprehensive One Health framework.