Spiroplasma shows a Wolbachia-like effect in hampering virus replication in spider mite

Background Members of the Acari order, commonly known as mites, play a significant role as agricultural pests. Among these, the Tetranychidae family stands out due to its remarkable diversity, surrounding approximately 1200 species capable of infesting over 4000 plant species. By feeding on plant tissues, these mites directly harm crops and can also serve as vectors for viral pathogens, posing a substantial threat to global food security. In this study, we investigated the unexplored virome of Tetranychus truncatus exploring how biotic factors (Spiroplasma and Wolbachia endosymbionts), and abiotic stresses (abamectin and temperature) affect virus dynamics. Results Our metatranscriptomics analyses revealed sequences related to important arthropod- and crop-infecting viral families, including the known plant-pathogenic Potato Y virus and Cherry A virus strains and fourteen new species. Notably, abamectin treatment correlated with the absence of Potato virus Y and TtDV-2 virus, suggesting this pesticide impacts viral diversity. Interestingly, single infections of Wolbachia or Spiroplasma significantly decreased both the diversity and the abundance of viruses, with the greatest effect on dicistroviruses, indicating for the first time the potential of Spiroplasma to restrict viral infections. Surprisingly, Wolbachia-Spiroplasma co-infection leads to the loss of the virus restriction effect. Wolbachia-exclusive and Spiroplasma-exclusive responsive genes showed enrichment for similar pathways, with piRNA and autophagy enriched in up-regulated genes. In contrast, lipid metabolic processes were enriched in down-regulated elements. Conclusions Overall, our study describes the T. truncatus virome, unveiling the considerable influence of its microbiome, including Wolbachia and Spiroplasma, and Abamectin pesticide on both virus diversity and abundance.