Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoes
ABSTRACT Climate change is predicted to increase the spread of mosquito-borne viruses, but genetic mechanisms underlying the influence of environmental variation on the ability of insect vectors to transmit human pathogens is unknown. In response to a changing climate, mosquitoes will experience lon...
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American Society for Microbiology
2025-03-01
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| Online Access: | https://journals.asm.org/doi/10.1128/mbio.01207-24 |
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| author | Anastasia Accoti Margaret Becker Angel Elma I. Abu Julia Vulcan Ruimei Jun Steven G. Widen Massamba Sylla Vsevolod L. Popov Laura B. Dickson |
| author_facet | Anastasia Accoti Margaret Becker Angel Elma I. Abu Julia Vulcan Ruimei Jun Steven G. Widen Massamba Sylla Vsevolod L. Popov Laura B. Dickson |
| author_sort | Anastasia Accoti |
| collection | DOAJ |
| description | ABSTRACT Climate change is predicted to increase the spread of mosquito-borne viruses, but genetic mechanisms underlying the influence of environmental variation on the ability of insect vectors to transmit human pathogens is unknown. In response to a changing climate, mosquitoes will experience longer periods of drought. An important physiological response to dry environments is the protection against dehydration, here defined as desiccation tolerance. While temperature is known to impact interactions between mosquito and virus, the role of dehydration remains unknown. We identified two genetically diverse lines of the mosquito Aedes aegypti, a major arbovirus vector, with marked differences in desiccation tolerance. To determine the genetic response to dehydration between these contrasting lines, we compared gene expression profiles between desiccant- and non-desiccant-treated individuals in both the desiccation-tolerant and -susceptible lines by RNAseq. Gene expression analysis demonstrated that several genes are differentially expressed in response to desiccation stress between desiccation-tolerant and -susceptible lines. The most highly expressed transcript under desiccation stress in the desiccation-susceptible line encodes a peritrophin protein, Ae-Aper50. Peritrophins play a crucial role in peritrophic matrix formation in the mosquito midgut after a bloodmeal. Gene silencing of Ae-Aper50 by RNAi demonstrated that expression of Ae-Aper50 is required for survival of the desiccation-susceptible line under desiccation stress, but not for the desiccation-tolerant line. Moreover, the knockdown of Ae-Aper50 resulted in higher Zika virus (ZIKV) infection rates in the desiccation-tolerant line and increased ZIKV viral replication in the desiccation susceptible line, and higher chikungunya virus (CHIKV) infection rates in the desiccation-tolerant line. Altogether, these results provide a link between protection against desiccation and midgut infection, which has important implications in predicting how climate change will impact mosquito-borne viruses.IMPORTANCEClimate change will have profound impacts on the burden of viruses transmitted by mosquitoes. While we know how changes in temperature impact mosquito physiology and dynamics of viral replication within the mosquito, there is a complete lack of knowledge in how low humidity, or drought tolerance, will impact interactions between mosquitoes and arboviruses. Understanding how drought tolerance will alter mosquito infection with arboviruses is critical in predicting and preventing the impact that climate change will have on mosquito-borne viruses. This work demonstrates a functional link between dehydration tolerance and midgut infection. This knowledge significantly enhances our understanding of how the predicted increase in droughts could impact the dynamics of mosquito-borne viruses. |
| format | Article |
| id | doaj-art-ef370a28a1e349cba8bb725a18d4e536 |
| institution | DOAJ |
| issn | 2150-7511 |
| language | English |
| publishDate | 2025-03-01 |
| publisher | American Society for Microbiology |
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| series | mBio |
| spelling | doaj-art-ef370a28a1e349cba8bb725a18d4e5362025-08-20T02:52:41ZengAmerican Society for MicrobiologymBio2150-75112025-03-0116310.1128/mbio.01207-24Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoesAnastasia Accoti0Margaret Becker1Angel Elma I. Abu2Julia Vulcan3Ruimei Jun4Steven G. Widen5Massamba Sylla6Vsevolod L. Popov7Laura B. Dickson8Department of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USADepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USADepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USADepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USADepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USADepartment of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, Texas, USALaboratory Vectors and Parasites, Department of Livestock Sciences and Techniques, Sine Saloum University El Hadji Ibrahima NIASS, Kaffrine Campus, Kaffrine, SenegalDepartment of Pathology, University of Texas Medical Branch, Galveston, Texas, USADepartment of Microbiology and Immunology, University of Texas Medical Branch, Galveston, Texas, USAABSTRACT Climate change is predicted to increase the spread of mosquito-borne viruses, but genetic mechanisms underlying the influence of environmental variation on the ability of insect vectors to transmit human pathogens is unknown. In response to a changing climate, mosquitoes will experience longer periods of drought. An important physiological response to dry environments is the protection against dehydration, here defined as desiccation tolerance. While temperature is known to impact interactions between mosquito and virus, the role of dehydration remains unknown. We identified two genetically diverse lines of the mosquito Aedes aegypti, a major arbovirus vector, with marked differences in desiccation tolerance. To determine the genetic response to dehydration between these contrasting lines, we compared gene expression profiles between desiccant- and non-desiccant-treated individuals in both the desiccation-tolerant and -susceptible lines by RNAseq. Gene expression analysis demonstrated that several genes are differentially expressed in response to desiccation stress between desiccation-tolerant and -susceptible lines. The most highly expressed transcript under desiccation stress in the desiccation-susceptible line encodes a peritrophin protein, Ae-Aper50. Peritrophins play a crucial role in peritrophic matrix formation in the mosquito midgut after a bloodmeal. Gene silencing of Ae-Aper50 by RNAi demonstrated that expression of Ae-Aper50 is required for survival of the desiccation-susceptible line under desiccation stress, but not for the desiccation-tolerant line. Moreover, the knockdown of Ae-Aper50 resulted in higher Zika virus (ZIKV) infection rates in the desiccation-tolerant line and increased ZIKV viral replication in the desiccation susceptible line, and higher chikungunya virus (CHIKV) infection rates in the desiccation-tolerant line. Altogether, these results provide a link between protection against desiccation and midgut infection, which has important implications in predicting how climate change will impact mosquito-borne viruses.IMPORTANCEClimate change will have profound impacts on the burden of viruses transmitted by mosquitoes. While we know how changes in temperature impact mosquito physiology and dynamics of viral replication within the mosquito, there is a complete lack of knowledge in how low humidity, or drought tolerance, will impact interactions between mosquitoes and arboviruses. Understanding how drought tolerance will alter mosquito infection with arboviruses is critical in predicting and preventing the impact that climate change will have on mosquito-borne viruses. This work demonstrates a functional link between dehydration tolerance and midgut infection. This knowledge significantly enhances our understanding of how the predicted increase in droughts could impact the dynamics of mosquito-borne viruses.https://journals.asm.org/doi/10.1128/mbio.01207-24climate changeArbovirusmosquito |
| spellingShingle | Anastasia Accoti Margaret Becker Angel Elma I. Abu Julia Vulcan Ruimei Jun Steven G. Widen Massamba Sylla Vsevolod L. Popov Laura B. Dickson Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoes mBio climate change Arbovirus mosquito |
| title | Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoes |
| title_full | Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoes |
| title_fullStr | Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoes |
| title_full_unstemmed | Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoes |
| title_short | Dehydration-induced Ae-Aper50 regulates midgut infection in Aedes aegypti mosquitoes |
| title_sort | dehydration induced ae aper50 regulates midgut infection in aedes aegypti mosquitoes |
| topic | climate change Arbovirus mosquito |
| url | https://journals.asm.org/doi/10.1128/mbio.01207-24 |
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