Potential Effect of Wolbachia on virus restriction in the spider mite Tetranychus truncatus

Lucas Yago Melo Ferreira¹João Pedro Nunes Santos¹David Gabriel do Nascimento Souza¹Lixsy Celeste Bernardez Orellana¹Sabrina Ferreira de Santana¹Anderson Gonçalves Sousa¹Paula Luize Camargos Fonseca²Amanda Gabrielly Santana Silva¹Vinicius Castro Santos²Isaque João Da Silva De Faria²Roenick Proveti Olmo³Luis Gustavo Carvalho Pacheco⁴Marcio G. C. Costa¹Carlos Priminho Pirovani¹Anibal Ramadan Oliveira¹Eric Roberto Guimarães Rocha Aguiar^1*

• ¹Universidade Estadual de Santa Cruz, Ilhéus, Brazil
• ²Minas Gerais State University, Belo Horizonte, Minas Gerais, Brazil
• ³FRC1589 Institut de Biologie Moléculaire et Cellulaire, Université de Strasbourg (IBMC), Strasbourg, Alsace, France
• ⁴Federal University of Bahia (UFBA), Salvador, Bahia, Brazil

The mite Tetranychus truncatus is a significant agricultural pest and may serve as a potential vector for viral transmission. However, the virome of T. truncatus remains understudied. Through metatranscriptomic analyses of publicly available data, we uncovered a diverse range of viruses associated with the spider mite, including crop-infecting pathogenic species such as Potato virus Y and Cherry virus A, and fourteen previously unknown viruses across several families (e.g., Virgaviridae, Dicistroviridae, Kitaviridae, Betaflexiviridae and Nudiviridae). Taking advantage of mite samples under different conditions, we also assessed the impact of biotic (Wolbachia and Spiroplasma infection) and abiotic stresses (pesticide exposure and temperature stress) on the T. truncatus virome. Interestingly, Wolbachia appeared to restrict viral infections in Tetranychus truncatus by reducing viral diversity and abundance, with a pronounced effect on dicistroviruses. Surprisingly, a similar effect also observed with Spiroplasma. However, the viral restriction phenotype vanishes in co-infected mites. Transcriptomics analysis of singly-infected mites revealed upregulation of piRNA and autophagy-related genes, while lipid metabolism processesrelated genes were downregulated, indicating an endosymbiont-sharing mechanisms of viral interference. Although the impact of abiotic stressors on the virome was not statistically significant, Potato virus Y and TtDV-2 viruses were absent in abamectin-exposed mites, suggesting a potential reduction in the viral diversity, while heat-stressed mites exhibited slightly higher viral diversity compared to those raised at regular temperatures. Overall, our work provides a detailed analysis of the T. truncatus virome, shedding light on how endosymbionts and environmental factors shape viral dynamics and offering potential insights for pest management strategies.