Metagenomics show high spatiotemporal virus diversity and ecological compartmentalisation: Virus infections of melon, Cucumis melo, crops, and adjacent wild communities

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The emergence of viral diseases results from novel transmission dynamics between wild and crop plant communities. The bias of studies towards pathogenic viruses of crops has distracted from knowledge of non-antagonistic symbioses in wild plants. Here, we implemented a high-throughput approach to compare the viromes of melon (Cucumis melo) and wild plants of crop (Crop) and adjacent boundaries (Edge). Each of the 41-plant species examined was infected by at least one virus. The interactions of 104 virus operational taxonomic units (OTUs) with these hosts occurred largely within ecological compartments of either Crop or Edge, with Edge having traits of a reservoir community. Local scale patterns of infection were characterised by the positive correlation between plant and virus richness at each site, the tendency for increased specialist host use through seasons, and specialist host use by OTUs observed only in Crop, characterised local-scale patterns of infection. In this study of systematically sampled viromes of a crop and adjacent wild communities, most hosts showed no disease symptoms, suggesting non-antagonistic symbioses are common. The coexistence of viruses within species-rich ecological compartments of agro-systems might promote the evolution of a diversity of virus strategies for survival and transmission. These communities, including those suspected as reservoirs, are subject to sporadic changes in assemblages, and so too are the conditions that favour the emergence of disease.

This work was funded in part by Plan Estatal de I+D+i, Ministerio de Economía y Competividad , Spain (grants BFU2015-64018-R and RTI2018-094302-B-I00) and by ArimNet2 2015 joint Call (project 618127, EMERAMB). A.P. was supported by a Formacion de Personal Investigador contract (BES-2016-077810). A.Z. and B.B. were supported by funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Sklodowska-Curie grant agreement No. 813542T INEXTVIR. We thank Dr Rosario Gavilán, Departamento de Farmacología, Farmacognosia y Botánica, Facultad de Farmacia, Universidad Complutense, Madrid, Spain, for the taxonomic identification of plant species. We also acknowledge the contribution of detailed recommendations and time spent by three anonymous reviewers, which improved the quality of the manuscript.

Peer reviewed