The genome of the biting midge Culicoides sonorensis and gene expression analyses of vector competence for Bluetongue virus

Authors: MORALES-HOJAS, RAMIRO - The Pirbright Institute; HINSLEY, MALCOLM - European Bioinformatics Institute; ARMEAN, IRINA - European Bioinformatics Institute; SILK, RHIANNON - The Pirbright Institute; HARRUP, LARA - The Pirbright Institute; GONZALEZ-URIARTE, ASIER - Rothamsted Research; VERONESI, EVA - The Pirbright Institute; CAMPBELL, LACHEN - European Bioinformatics Institute; Nayduch, Dana; SASKI, CHRISTOPHER - Clemson University; TABACHNICK, WALTER - Florida Medical Entomology Laboratory; KERSEY, PAUL - European Bioinformatics Institute; CARPENTER, SIMON - The Pirbright Institute; FIFE, MARK - The Pirbright Institute

Submitted to: BMC Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/14/2018
Publication Date: 8/22/2018
Citation: Morales-Hojas, R., Hinsley, M., Armeam, I., Silk, R., Harrup, L., Gonzalez-Uriarte, A., Veronesi, E., Campbell, L., Nayduch, D., Saski, C., Tabachnick, W., Kersey, P., Carpenter, S., Fife, M. 2018. The genome of the biting midge Culicoides sonorensis and gene expression analyses of vector competence for Bluetongue virus. BMC Genomics. 19:624. https://doi.org/10.1101/249482.
DOI: https://doi.org/10.1101/249482

Interpretive Summary: Biting midges of the genus Culicoides transmit some of the most important arboviruses of wildlife and livestock worldwide, with a global impact on economic productivity, health and welfare. The absence of a suitable reference genome has hindered genomic analyses to date in this important vector. Here we present the genome of Culicoides sonorensis, a vector of bluetongue virus (BTV) and epizootic hemorrhagic disease virus (EHDV) in the USA. The genome size is 197.4 Mb and contains 15,629 identified genes. Transcriptome analysis revealed 165 genes that were differentially expressed between female C. sonorensis females that were permissive vs. refractory to infection with BTV. Two candidate genes, glutathione S-transferase (gst) and the antiviral helicase ski2, previously recognized as involved in vector competence for BTV in C. sonorensis (gst) and repressing dsRNA virus propagation (ski2), were confirmed in this study. The reference genome of C. sonorensis has enabled preliminary analyses of the gene expression profiles of vector competent and refractory individuals. The genome and transcriptomes generated in this study provide suitable tools for future research on arbovirus transmission. The genome and transcriptomes provide a significant resource for researchers studying Culicoides and other insects within this vector lineage, which diverged from other major Dipteran vector families (such as mosquitoes) over 200 million years ago. The genome will be a valuable source of comparative analyses with other important vectors such as mosquitoes and sandflies and can yield potential targets for transgenic modification in vector control and functional studies.

Technical Abstract: Background: The use of the new genomic technologies has led to major advances in control of several arboviruses of medical importance such as Dengue. However, the development of tools and resources available for vectors of non-zoonotic arboviruses remains neglected. Biting midges of the genus Culicoides transmit some of the most important arboviruses of wildlife and livestock worldwide, with a global impact on economic productivity, health and welfare. The absence of a suitable reference genome has hindered genomic analyses to date in this important genus of vectors. In the present study, the genome of Culicoides sonorensis, a vector of bluetongue virus (BTV) in the USA, has been sequenced to provide the first reference genome for these vectors. In this study, we also report the use of the reference genome to perform initial transcriptomic analyses of vector competence for BTV. Results: Our analyses reveal that the genome is 197.4 Mb, assembled in 7,974 scaffolds. Its annotation using the transcriptomic data generated in this study and in a previous study has identified 15,629 genes. Gene expression analyses of C. sonorensis females infected with BTV performed in this study revealed 165 genes that were differentially expressed between vector competent and refractory females. Two candidate genes, glutathione S-transferase (gst) and the antiviral helicase ski2, previously recognized as involved in vector competence for BTV in C. sonorensis (gst) and repressing dsRNA virus propagation (ski2), were confirmed in this study. Conclusions: The reference genome of C. sonorensis has enabled preliminary analyses of the gene expression profiles of vector competent and refractory individuals. The genome and transcriptomes generated in this study provide suitable tools for future research on arbovirus transmission. These provide a significant resource for these vector lineage, which diverged from other major Dipteran vector families over 200 million years ago. The genome will be a valuable source of comparative data for other important Dipteran vector families including mosquitoes (Culicidae) and sandflies (Psychodidae), and yield potential targets for transgenic modification in vector control and functional studies.