Diversity and persistence of the RNA virome of Philaenus spumarius, the European vector of Xylella fastidiosa

Philaenus spumarius is the primary vector of the quarantine plant pathogen Xylella fastidiosa in Europe and is responsible for the devastating Olive Quick Decline Syndrome outbreak in Southern Italy. Despite its importance, little is known about its natural viral community, which could offer novel and sustainable strategies for vector control. In this three-year study, we conducted the first comprehensive characterization of the viral community of P. spumarius from multiple ecologically diverse European sites, including X. fastidiosa-affected areas in Southern Italy. Deep transcriptomic sequencing of 209 field-collected individuals pooled into 11 RNA-seq libraries revealed the presence of 26 RNA viruses. Our findings revealed a rich and structured viral community in populations from Northern Italy and France, contrasting sharply with the reduced viral diversity observed in populations from Southern Italy, where most individuals were virus-free. Temporal comparisons revealed recurrent virus-host associations over the years, and laboratory rearing provided initial insights into viral persistence and transmission dynamics. Although none of the detected viruses caused overt signs of mortality or sterility, their potential sublethal effects and ecological interactions remain unexplored. This study lays the groundwork for future research on the functional roles of insect-associated viruses and emphasizes their potential for developing sustainable, environmentally friendly approaches to managing vectors and reducing the impact of X. fastidiosa on European agriculture.