The chromosome-scale genome assembly for the West Nile vector Culex quinquefasciatus uncovers patterns of genome evolution in mosquitoes

Author:

Ryazansky Sergei S.,Chen Chujia,Potters Mark,Naumenko Anastasia N.,Lukyanchikova Varvara,Masri Reem A.,Brusentsov Ilya I.,Karagodin Dmitriy A.,Yurchenko Andrey A.,dos Anjos Vitor L.,Haba Yuki,Rose Noah H.,Hoffman Jinna,Guo Rong,Menna Theresa,Kelley Melissa,Ferrill Emily,Schultz Karen E.,Qi Yumin,Sharma Atashi,Deschamps Stéphane,Llaca Victor,Mao Chunhong,Murphy Terence D.,Baricheva Elina M.,Emrich Scott,Fritz Megan L.,Benoit Joshua B.,Sharakhov Igor V.,McBride Carolyn S.,Tu Zhijian,Sharakhova Maria V.ORCID

Abstract

Abstract Background Understanding genome organization and evolution is important for species involved in transmission of human diseases, such as mosquitoes. Anophelinae and Culicinae subfamilies of mosquitoes show striking differences in genome sizes, sex chromosome arrangements, behavior, and ability to transmit pathogens. However, the genomic basis of these differences is not fully understood. Methods In this study, we used a combination of advanced genome technologies such as Oxford Nanopore Technology sequencing, Hi-C scaffolding, Bionano, and cytogenetic mapping to develop an improved chromosome-scale genome assembly for the West Nile vector Culex quinquefasciatus. Results We then used this assembly to annotate odorant receptors, odorant binding proteins, and transposable elements. A genomic region containing male-specific sequences on chromosome 1 and a polymorphic inversion on chromosome 3 were identified in the Cx. quinquefasciatus genome. In addition, the genome of Cx. quinquefasciatus was compared with the genomes of other mosquitoes such as malaria vectors An. coluzzi and An. albimanus, and the vector of arboviruses Ae. aegypti. Our work confirms significant expansion of the two chemosensory gene families in Cx. quinquefasciatus, as well as a significant increase and relocation of the transposable elements in both Cx. quinquefasciatus and Ae. aegypti relative to the Anophelines. Phylogenetic analysis clarifies the divergence time between the mosquito species. Our study provides new insights into chromosomal evolution in mosquitoes and finds that the X chromosome of Anophelinae and the sex-determining chromosome 1 of Culicinae have a significantly higher rate of evolution than autosomes. Conclusion The improved Cx. quinquefasciatus genome assembly uncovered new details of mosquito genome evolution and has the potential to speed up the development of novel vector control strategies.

Funder

Division of Intramural Research, National Institute of Allergy and Infectious Diseases

Russian Science Foundation

New York Stem Cell Foundation

National Institute of Food and Agriculture

Tomsk State University

NCBI, NLM, NIH

Institute of Cytology and Genetics SBRAS, Russia

Publisher

Springer Science and Business Media LLC

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