TY - JOUR

T1 - The chromosome-scale genome assembly for the West Nile vector Culex quinquefasciatus uncovers patterns of genome evolution in mosquitoes

AU - Ryazansky, Sergei S

AU - Chen, Chujia

AU - Potters, Mark

AU - Naumenko, Anastasia N

AU - Lukyanchikova, Varvara

AU - Masri, Reem A

AU - Brusentsov, Ilya I

AU - Karagodin, Dmitriy A

AU - Yurchenko, Andrey A

AU - Dos Anjos, Vitor L

AU - Haba, Yuki

AU - Rose, Noah H

AU - Hoffman, Jinna

AU - Guo, Rong

AU - Menna, Theresa

AU - Kelley, Melissa

AU - Ferrill, Emily

AU - Schultz, Karen E

AU - Qi, Yumin

AU - Sharma, Atashi

AU - Deschamps, Stéphane

AU - Llaca, Victor

AU - Mao, Chunhong

AU - Murphy, Terence D

AU - Baricheva, Elina M

AU - Emrich, Scott

AU - Fritz, Megan L

AU - Benoit, Joshua B

AU - Sharakhov, Igor V

AU - McBride, Carolyn S

AU - Tu, Zhijian

AU - Sharakhova, Maria V

N1 - The project was supported by multiple funding sources. Genome assembly and analysis was funded in part by NIH/NIAID grants AI154871 to Z.T. BAC clone sequencing and physical mapping was supported by NIH/NIAID grant AI156280 to M.V.S. and AI123967 to S.E. Hi-C scaffolding, TE annotation, and comparative genomics was supported by the Russian Science Foundation grant 19-14-00130 to M.V.S. and by the FWNR-2022-0015 project of the Institute of Cytology and Genetics. Odorant receptor analysis and annotation was supported by a grant from the New York Stem Cell Foundation to CSM. CMS is a New York Stem Cell Foundation – Robertson Investigator. Partial support was provided by the NIH/NIAID grant AI176098 and AI148551 for tRNA and RNA-seq analyses to J.B.B. and M.K. Chromosome evolution analysis was partly supported by the USDA National Institute of Food and Agriculture Hatch project VA-160179 and VA-160058 to I.V.S. and M.V.S. and by the Tomsk State University Development Programme (Priority-2030) to I.V.S. The work of J.H. and T.D.M. was supported by the National Center for Biotechnology Information of the National Library of Medicine (NLM), National Institutes of Health. © 2024. The Author(s).

PY - 2024/12

Y1 - 2024/12

N2 - 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.

AB - 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.

KW - Animals

KW - Humans

KW - Male

KW - Phylogeny

KW - DNA Transposable Elements/genetics

KW - Mosquito Vectors/genetics

KW - Culex/genetics

KW - Aedes/genetics

KW - Chromosomes

KW - Evolution, Molecular

UR - https://www.scopus.com/record/display.uri?eid=2-s2.0-85183001740&origin=inward&txGid=6cac3234a94d38f29768379f73ccd8cf

U2 - 10.1186/s12915-024-01825-0

DO - 10.1186/s12915-024-01825-0

M3 - Article

C2 - 38273363

VL - 22

JO - BMC Biology

JF - BMC Biology

SN - 1741-7007

IS - 1

M1 - 16

ER -