Complexity and local specificity of the virome associated with tospovirus-transmitting thrips species

SUMMARY Frankliniella occidentalis (western flower thrips [WFT]) and Thrips tabaci (onion thrips [OT]) are insect species that greatly impact horticultural crops through direct damage and their efficient vectoring of tomato spotted wilt virus and iris yellow spot virus. In this study, we collected thrips of these species from 12 field populations in various regions in Italy. We also included one field population of Neohydatothrips variabilis (soybean thrips [ST]) from the United States. Total RNA data from high-throughput sequencing (HTS) were used to assemble the virome, and then we assigned putative viral contigs to each thrips sample by real-time reverse transcription-quantitative PCR (qRT-PCR). Excluding plant and fungal viruses, we were able to identify 61 viral segments, corresponding to 41 viruses: 14 were assigned to WFT, 17 to OT, and 1 to ST; 9 viruses could not be assigned to any species based on our stringent criteria. All these viruses are putative representative of new species (with only the exception of a sobemo-like virus that is 100% identical to a virus recently characterized in ST) and some belong to new higher-ranking taxa. These additions to the viral phylogeny suggest previously undescribed evolutionary niches. Most of Baltimore's classes of RNA viruses were present (positive- and minus-strand and double-stranded RNA viruses), but only one DNA virus was identified in our collection. Repeated sampling in a subset of locations in 2019 and 2020 and further virus characterization in a subset of four thrips populations maintained in the laboratory allowed us to provide evidence of a locally persistent thrips core virome that characterizes each population. IMPORTANCE Harnessing the insect microbiome can result in new approaches to contain their populations or the damage they cause vectoring viruses of medical, veterinary, or agricultural importance. Persistent insect viruses are a neglected component of their microbiota. In this study, for the first time, we characterize the virome associated with the two model systems for tospovirus-transmitting thrips species, of utmost importance for the direct and indirect damage they cause to a number of different crops. The thrips virome characterized includes several novel viruses, which in some cases reveal previously undescribed clades. More importantly, some of the viruses we describe are part of a core virome that is specific and consistently present in distinct geographical locations monitored over the years, hinting at a possible mutualistic symbiotic relationship with their host.