Ever-increasing viral diversity associated with the red imported fire ant Solenopsis invicta (Formicidae: Hymenoptera)

Authors: XAVIER, CÉSAR - North Carolina State University; Allen, Margaret - Meg; WHITFIELD, ANNA - North Carolina State University

Submitted to: Virology Journal
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/9/2020
Publication Date: 1/6/2021
Publication URL: https://handle.nal.usda.gov/10113/7226989
Citation: Xavier, C.A., Allen, M.L., Whitfield, A.E. 2021. Ever-increasing viral diversity associated with the red imported fire ant Solenopsis invicta (Formicidae: Hymenoptera). Virology Journal. 18:5. https://doi.org/10.1186/s12985-020-01469-w.
DOI: https://doi.org/10.1186/s12985-020-01469-w

Interpretive Summary: Many new viruses have been discovered in insects recently. Some of these viruses cause insect diseases, while others appear to be benign. While viruses that cause insect diseases have obvious potential as insect pest control tools, those that infect pest insects without apparent disease symptoms may also be exploited as research tools, and, with some modification, in next-generation pest control. Invasive ants, and especially red imported fire ants, have spread worldwide and cause extensive damage. Examination of genetic materials from red imported fire ants established in different geographic locations revealed five new viruses. These new viruses provide insight on how invasive ants lose and acquire virus infections in new territories and may serve as tools to develop viral pest control products.

Technical Abstract: Background: Advances in sequencing and analysis tools have facilitated discovery of many new viruses from invertebrates, including ants. Solenopsis invicta is an invasive ant that has quickly spread around world causing significant ecological and economic impacts. Its virome has begun to be characterized pertaining to potential use of viruses as a natural enemy. Although the S. invicta virome is the best characterized among ants, most studies have been performed in its native range, with little information from invaded areas. Methods: In the present study, using a metatranscriptome approach, we further characterized viruses associated with S. invicta, in two introduced areas, U.S and Taiwan. The data set used here was obtained from different stages (larvae, pupa, and adults) of the S. invicta life cycle. Publicly available RNA sequences from GenBank’s Sequence Read Archive were downloaded and de novo assembled using CLC Genomics Workbench 20.0.1. Contigs were compared against the non-redundant protein sequences and those showing similarity to viral sequences were further analyzed. Results: We characterized five putative new viruses associated with the S. invicta transcriptomes. Sequence comparisons revealed extensive divergence across ORFs and genomic regions with most of them sharing less than 40% amino acid identity with those closest homologous sequences previously characterized. The first negative-sense single-stranded RNA viruses included in the orders Bunyavirales and Mononegavirales are reported. In addition, two positive single-strand viruses and one single strand DNA virus were also characterized. While the presence of a putative tenuivirus associated to S. invicta was previously suggested to be a contamination, here we characterized and present strong evidence that SINV-14 is a tenui-like virus that has a long-term association with the ant. Furthermore, based on virus abundance compared to housekeeping genes, phylogenetic relationships, and completeness of viral coding sequences, our results suggest that four of five viruses reported, those being SINV-14, SINV-15, SINV-16 and SINV-17, replicate in the ant S. invicta. Conclusions: The present study expands our knowledge about viral diversity associated with S. invicta in introduced areas with potential to be used as biological control agents, which will require further biological characterization.