Virome analysis reveals an arthropod-specific RNA virus that enhances host adaptation to stress

Viruses are obligate parasites that rely on host cellular machinery for replication and transmission. Accordingly, arthropod-associated viruses can establish neutral, beneficial, or pathogenic relationships. However, over the past two decades, metatranscriptome studies have uncovered diverse viromes that include many asymptomatic RNA viruses. Here we focus on newly discovered arthropod-specific RNA viruses whose biological functions and ecological significance remain largely unknown. We analyzed the virome of the two-spotted mite Tetranychus urticae , a globally distributed agricultural pest that infests more than 1100 plants. Among 153 transcriptome datasets, we identified five novel putative viral sequences. Together with all previously reported viruses in T. urticae , we took the 22 viruses as the whole virome and analyzed their dynamics across all 515 transcriptome datasets in NCBI, finding an average of five viruses per dataset. The most prevalent were Tetranychus urticae Nege/Kita-like virus (TuNKV) and Tetranychus urticae dicistro-like virus 1 (TuDV-1). These viruses also triggered robust RNAi responses in four field-collected mite populations, implying they are infectious. Intriguingly, TuNKV was asymptomatic but significantly enhanced host adaptation to abiotic and biotic stresses. We found that TuNKV structural protein 24 (SP24) interacted with host cuticle proteins (CPRs), and that silencing the CPRs also reduced viral titers and diminished the protection induced by TuNKV. Importantly, TuNKV enhanced host population growth during an ecological bottleneck caused by combined stress challenges. Our study demonstrates that viral reads account for a significant fraction of the T. urticae transcriptome and represent prevalent viruses with ecological relevance. In particular, TuNKV appears to enhance host survival during exposure to diverse environmental stresses. Moving beyond the conventional view of viruses solely as a burden to their hosts, these findings expand our knowledge of arthropod viruses and host–virus relationships. Video Abstract