Increase of niche filling with increase of host richness for plant-infecting mastreviruses

Virus Evol. 2024 Dec 13;10(1):veae107. doi: 10.1093/ve/veae107. eCollection 2024.

Abstract

Now that it has been realized that viruses are ubiquitous, questions have been raised on factors influencing their diversity and distribution. For phytoviruses, understanding the interplay between plant diversity and virus species richness and prevalence remains cardinal. As both the amplification and the dilution of viral species richness due to increasing host diversity have been theorized and observed, a deeper understanding of how plants and viruses interact in natural environments is needed to explore how host availability conditions viral diversity and distributions. From a unique dataset, this study explores interactions of Mastrevirus species (family Geminiviridae) with Poales order hosts across 10 sites from three contrasting ecosystems on La Réunion. Among 273 plant pools, representing 61 Poales species, 15 Mastrevirus species were characterized from 22 hosts. The analysis revealed a strong association of mastreviruses with hosts from agroecosystems, the rare presence of viruses in coastal grasslands, and the absence of mastreviruses in subalpine areas, areas dominated by native plants. This suggests that detected mastreviruses were introduced through anthropogenic activities, emphasizing the role of humans in shaping the global pathobiome. By reconstructing the realized host-virus infection network, besides revealing a pattern of increasing viral richness with increasing host richness, we observed increasing viral niche occupancies with increasing host species richness, implying that virus realized richness at any given site is conditioned on the global capacity of the plant populations to host diverse mastreviruses. Whether this tendency is driven by synergy between viruses or by an interplay between vector population and plant richness remains to be established.

Keywords: Mastrevirus; Poales; agroecosystem; ecology; host–pathogen interaction network; viral metagenomics.