Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposure

Abstract Background Malaria remains a key contributor to mortality and morbidity across Africa, with the highest burden in children under 5. Insecticide-based vector control tools, which target the adult Anopheles mosquitoes, are the most efficacious tool in disease prevention. Due to the widespread...

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Main Authors: Netsanet Worku, Antoine Sanou, Juliane Hartke, Marion Morris, Fatoumata Cissé, Salimata Ouédraogo, Madou Tapsoba, Nicola Vallon, Tewodros Debebe Akilu, Ligabaw Worku, Moussa Wamdaogo Guelbeogo, Victoria A. Ingham
Format: Article
Language:English
Published: BMC 2025-01-01
Series:Parasites & Vectors
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Online Access:https://doi.org/10.1186/s13071-024-06638-2
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author Netsanet Worku
Antoine Sanou
Juliane Hartke
Marion Morris
Fatoumata Cissé
Salimata Ouédraogo
Madou Tapsoba
Nicola Vallon
Tewodros Debebe Akilu
Ligabaw Worku
Moussa Wamdaogo Guelbeogo
Victoria A. Ingham
author_facet Netsanet Worku
Antoine Sanou
Juliane Hartke
Marion Morris
Fatoumata Cissé
Salimata Ouédraogo
Madou Tapsoba
Nicola Vallon
Tewodros Debebe Akilu
Ligabaw Worku
Moussa Wamdaogo Guelbeogo
Victoria A. Ingham
author_sort Netsanet Worku
collection DOAJ
description Abstract Background Malaria remains a key contributor to mortality and morbidity across Africa, with the highest burden in children under 5. Insecticide-based vector control tools, which target the adult Anopheles mosquitoes, are the most efficacious tool in disease prevention. Due to the widespread use of these interventions, insecticide resistance to the most used classes of insecticides is now pervasive across Africa. Understanding the underlying mechanisms contributing to this phenotype is necessary to both track the spread of resistance and to design new tools to overcome it. Methods Here, we compare the microbiota composition of insecticide-resistant populations of Anopheles gambiae, An. coluzzii and An. arabiensis from Burkina Faso, and in the latter case additionally from Ethiopia, to insecticide-susceptible populations. Results We show that the microbiota composition between insecticide-resistant and -susceptible populations does not differ in Burkina Faso. This result is supported by data from laboratory colonies originating in Burkina Faso across two countries. In contrast, An. arabiensis from Ethiopia demonstrates clear differences in microbiota composition in those dying from and those surviving insecticide exposure. To further understand resistance in this An. arabiensis population, we performed RNAseq and saw differential expression of detoxification genes associated with insecticide resistance and changes in respiration, metabolism and synapse-related ion channels. Conclusions Our results indicate that, in addition to changes in the transcriptome, microbiota can contribute to insecticide resistance in certain settings. Graphical Abstract
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spelling doaj-art-db411225792a4e63a3929bee1cf86d8e2025-01-26T12:17:41ZengBMCParasites & Vectors1756-33052025-01-0118111410.1186/s13071-024-06638-2Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposureNetsanet Worku0Antoine Sanou1Juliane Hartke2Marion Morris3Fatoumata Cissé4Salimata Ouédraogo5Madou Tapsoba6Nicola Vallon7Tewodros Debebe Akilu8Ligabaw Worku9Moussa Wamdaogo Guelbeogo10Victoria A. Ingham11Institute of Public Health (IPH), College of Medicine and Health Sciences, University of GondarCentre National de Recherche et de Formation sur le Paludisme (CNRFP)University Hospital Heidelberg, Medical Faculty, Centre for Infectious Diseases, Heidelberg UniversityVector Biology Department, Liverpool School of Tropical MedicineCentre National de Recherche et de Formation sur le Paludisme (CNRFP)Centre National de Recherche et de Formation sur le Paludisme (CNRFP)Centre National de Recherche et de Formation sur le Paludisme (CNRFP)University Hospital Heidelberg, Medical Faculty, Centre for Infectious Diseases, Heidelberg UniversityBIOMES NGS GmbHDepartment of Parasitology, School of Biomedical Sciences, College of Medicine and Health Sciences, University of GondarCentre National de Recherche et de Formation sur le Paludisme (CNRFP)University Hospital Heidelberg, Medical Faculty, Centre for Infectious Diseases, Heidelberg UniversityAbstract Background Malaria remains a key contributor to mortality and morbidity across Africa, with the highest burden in children under 5. Insecticide-based vector control tools, which target the adult Anopheles mosquitoes, are the most efficacious tool in disease prevention. Due to the widespread use of these interventions, insecticide resistance to the most used classes of insecticides is now pervasive across Africa. Understanding the underlying mechanisms contributing to this phenotype is necessary to both track the spread of resistance and to design new tools to overcome it. Methods Here, we compare the microbiota composition of insecticide-resistant populations of Anopheles gambiae, An. coluzzii and An. arabiensis from Burkina Faso, and in the latter case additionally from Ethiopia, to insecticide-susceptible populations. Results We show that the microbiota composition between insecticide-resistant and -susceptible populations does not differ in Burkina Faso. This result is supported by data from laboratory colonies originating in Burkina Faso across two countries. In contrast, An. arabiensis from Ethiopia demonstrates clear differences in microbiota composition in those dying from and those surviving insecticide exposure. To further understand resistance in this An. arabiensis population, we performed RNAseq and saw differential expression of detoxification genes associated with insecticide resistance and changes in respiration, metabolism and synapse-related ion channels. Conclusions Our results indicate that, in addition to changes in the transcriptome, microbiota can contribute to insecticide resistance in certain settings. Graphical Abstracthttps://doi.org/10.1186/s13071-024-06638-2AnophelesMalariaMicrobiomeInsecticide resistanceTranscriptomicsMicrobiota
spellingShingle Netsanet Worku
Antoine Sanou
Juliane Hartke
Marion Morris
Fatoumata Cissé
Salimata Ouédraogo
Madou Tapsoba
Nicola Vallon
Tewodros Debebe Akilu
Ligabaw Worku
Moussa Wamdaogo Guelbeogo
Victoria A. Ingham
Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposure
Parasites & Vectors
Anopheles
Malaria
Microbiome
Insecticide resistance
Transcriptomics
Microbiota
title Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposure
title_full Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposure
title_fullStr Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposure
title_full_unstemmed Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposure
title_short Insecticide resistant Anopheles from Ethiopia but not Burkina Faso show a microbiota composition shift upon insecticide exposure
title_sort insecticide resistant anopheles from ethiopia but not burkina faso show a microbiota composition shift upon insecticide exposure
topic Anopheles
Malaria
Microbiome
Insecticide resistance
Transcriptomics
Microbiota
url https://doi.org/10.1186/s13071-024-06638-2
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