Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral Reassortment

Rift Valley fever phlebovirus (RVFV) is a zoonotic mosquito-borne pathogen endemic to sub-Saharan Africa and the Arabian Peninsula which causes Rift Valley fever in ruminant livestock and humans. Co-infection with divergent viral strains can produce reassortment among the L, S, and M segments of the...

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Main Authors: Emma K. Harris, Velmurugan Balaraman, Cassidy C. Keating, Chester McDowell, J. Brian Kimble, Alina De La Mota-Peynado, Erin M. Borland, Barbara Graham, William C. Wilson, Juergen A. Richt, Rebekah C. Kading, Natasha N. Gaudreault
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Language:English
Published: MDPI AG 2025-01-01
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Online Access:https://www.mdpi.com/1999-4915/17/1/88
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author Emma K. Harris
Velmurugan Balaraman
Cassidy C. Keating
Chester McDowell
J. Brian Kimble
Alina De La Mota-Peynado
Erin M. Borland
Barbara Graham
William C. Wilson
Juergen A. Richt
Rebekah C. Kading
Natasha N. Gaudreault
author_facet Emma K. Harris
Velmurugan Balaraman
Cassidy C. Keating
Chester McDowell
J. Brian Kimble
Alina De La Mota-Peynado
Erin M. Borland
Barbara Graham
William C. Wilson
Juergen A. Richt
Rebekah C. Kading
Natasha N. Gaudreault
author_sort Emma K. Harris
collection DOAJ
description Rift Valley fever phlebovirus (RVFV) is a zoonotic mosquito-borne pathogen endemic to sub-Saharan Africa and the Arabian Peninsula which causes Rift Valley fever in ruminant livestock and humans. Co-infection with divergent viral strains can produce reassortment among the L, S, and M segments of the RVFV genome. Reassortment events can produce novel genotypes with altered virulence, transmission dynamics, and/or mosquito host range. This can have severe implications in areas where RVFV is endemic and convolutes our ability to anticipate transmission and circulation in novel geographic regions. Previously, we evaluated the frequency of RVFV reassortment in a susceptible ruminant host and observed low rates of reassortment (0–1.7%). Here, we tested the hypothesis that reassortment occurs predominantly in the mosquito using a highly permissive vector, <i>Culex tarsalis</i>. Cells derived from <i>Cx. tarsalis</i> or adult mosquitoes were co-infected with either two virulent (Kenya-128B-15 and SA01-1322) or a virulent and attenuated (Kenya-128B-15 and MP-12) strain of RVFV. Our results showed approximately 2% of virus genotypes isolated from co-infected <i>Cx. tarsalis</i>-derived cells were reassortant. Co-infected mosquitoes infected via infectious bloodmeal resulted in a higher percentage of reassortant virus (2–60%) isolated from midgut and salivary tissues at 14 days post-infection. The percentage of reassortant genotypes isolated from the midguts of mosquitoes co-infected with Kenya-128B-15 and SA01-1322 was similar to that of mosquitoes co-infected with Kenya-128B-15 and MP-12- strains (60 vs. 47%). However, only 2% of virus isolated from the salivary glands of Kenya-128B-15 and SA01-1322 co-infected mosquitoes represented reassortant genotypes. This was contrasted by 54% reassortment in the salivary glands of mosquitoes co-infected with Kenya-128B-15 and MP-12 strains. Furthermore, we observed preferential inclusion of genomic segments from the three parental strains among the reassorted viruses. Replication curves of select reassorted genotypes were significantly higher in Vero cells but not in <i>Culex</i>—derived cells. These data imply that mosquitoes play a crucial role in the reassortment of RVFV and potentially contribute to driving evolution of the virus.
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spelling doaj-art-7f9bdff72ebe4a868e15549f105c660f2025-01-24T13:52:33ZengMDPI AGViruses1999-49152025-01-011718810.3390/v17010088Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral ReassortmentEmma K. Harris0Velmurugan Balaraman1Cassidy C. Keating2Chester McDowell3J. Brian Kimble4Alina De La Mota-Peynado5Erin M. Borland6Barbara Graham7William C. Wilson8Juergen A. Richt9Rebekah C. Kading10Natasha N. Gaudreault11Center for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USACenter of Excellence for Emerging and Zoonotic Animal Diseases, Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, KS 66506, USACenter of Excellence for Emerging and Zoonotic Animal Diseases, Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, KS 66506, USACenter of Excellence for Emerging and Zoonotic Animal Diseases, Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, KS 66506, USAForeign Arthropod-Borne Animal Diseases Research Unit, United States Department of Agriculture, Agricultural Research Service, National Bio and Agro-Defense Facility, Manhattan, KS 66505, USAForeign Arthropod-Borne Animal Diseases Research Unit, United States Department of Agriculture, Agricultural Research Service, National Bio and Agro-Defense Facility, Manhattan, KS 66505, USACenter for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USACenter for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USAForeign Arthropod-Borne Animal Diseases Research Unit, United States Department of Agriculture, Agricultural Research Service, National Bio and Agro-Defense Facility, Manhattan, KS 66505, USACenter of Excellence for Emerging and Zoonotic Animal Diseases, Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, KS 66506, USACenter for Vector-Borne Infectious Diseases, Department of Microbiology, Immunology and Pathology, Colorado State University, Fort Collins, CO 80523, USACenter of Excellence for Emerging and Zoonotic Animal Diseases, Diagnostic Medicine/Pathobiology, Kansas State University, Manhattan, KS 66506, USARift Valley fever phlebovirus (RVFV) is a zoonotic mosquito-borne pathogen endemic to sub-Saharan Africa and the Arabian Peninsula which causes Rift Valley fever in ruminant livestock and humans. Co-infection with divergent viral strains can produce reassortment among the L, S, and M segments of the RVFV genome. Reassortment events can produce novel genotypes with altered virulence, transmission dynamics, and/or mosquito host range. This can have severe implications in areas where RVFV is endemic and convolutes our ability to anticipate transmission and circulation in novel geographic regions. Previously, we evaluated the frequency of RVFV reassortment in a susceptible ruminant host and observed low rates of reassortment (0–1.7%). Here, we tested the hypothesis that reassortment occurs predominantly in the mosquito using a highly permissive vector, <i>Culex tarsalis</i>. Cells derived from <i>Cx. tarsalis</i> or adult mosquitoes were co-infected with either two virulent (Kenya-128B-15 and SA01-1322) or a virulent and attenuated (Kenya-128B-15 and MP-12) strain of RVFV. Our results showed approximately 2% of virus genotypes isolated from co-infected <i>Cx. tarsalis</i>-derived cells were reassortant. Co-infected mosquitoes infected via infectious bloodmeal resulted in a higher percentage of reassortant virus (2–60%) isolated from midgut and salivary tissues at 14 days post-infection. The percentage of reassortant genotypes isolated from the midguts of mosquitoes co-infected with Kenya-128B-15 and SA01-1322 was similar to that of mosquitoes co-infected with Kenya-128B-15 and MP-12- strains (60 vs. 47%). However, only 2% of virus isolated from the salivary glands of Kenya-128B-15 and SA01-1322 co-infected mosquitoes represented reassortant genotypes. This was contrasted by 54% reassortment in the salivary glands of mosquitoes co-infected with Kenya-128B-15 and MP-12 strains. Furthermore, we observed preferential inclusion of genomic segments from the three parental strains among the reassorted viruses. Replication curves of select reassorted genotypes were significantly higher in Vero cells but not in <i>Culex</i>—derived cells. These data imply that mosquitoes play a crucial role in the reassortment of RVFV and potentially contribute to driving evolution of the virus.https://www.mdpi.com/1999-4915/17/1/88Rift Valley fever phlebovirusbunyavirus<i>Culex tarsalis</i>mosquitoreassortment
spellingShingle Emma K. Harris
Velmurugan Balaraman
Cassidy C. Keating
Chester McDowell
J. Brian Kimble
Alina De La Mota-Peynado
Erin M. Borland
Barbara Graham
William C. Wilson
Juergen A. Richt
Rebekah C. Kading
Natasha N. Gaudreault
Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral Reassortment
Viruses
Rift Valley fever phlebovirus
bunyavirus
<i>Culex tarsalis</i>
mosquito
reassortment
title Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral Reassortment
title_full Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral Reassortment
title_fullStr Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral Reassortment
title_full_unstemmed Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral Reassortment
title_short Co-Infection of <i>Culex tarsalis</i> Mosquitoes with Rift Valley Fever Phlebovirus Strains Results in Efficient Viral Reassortment
title_sort co infection of i culex tarsalis i mosquitoes with rift valley fever phlebovirus strains results in efficient viral reassortment
topic Rift Valley fever phlebovirus
bunyavirus
<i>Culex tarsalis</i>
mosquito
reassortment
url https://www.mdpi.com/1999-4915/17/1/88
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