First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional study

Abstract Background Recently, bacterial endosymbiont, including Wolbachia and Microsporidia were found to limit the infection of Anopheles mosquitoes with Plasmodium falciparum. This study aimed to investigate the natural presence of key transmission-blocking endosymbionts in Anopheles gambiae and A...

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Main Authors: Minassou Juvénal Ahouandjinou, Arthur Sovi, Aboubakar Sidick, Wilfried Sewadé, Come Zinsou Koukpo, Saïd Chitou, Linda Towakinou, Bruno Adjottin, Steve Hougbe, Filémon Tokponnon, Germain Gil Padonou, Martin Akogbéto, Louisa A. Messenger, Razaki A. Ossè
Format: Article
Language:English
Published: BMC 2024-03-01
Series:Malaria Journal
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Online Access:https://doi.org/10.1186/s12936-024-04906-1
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author Minassou Juvénal Ahouandjinou
Arthur Sovi
Aboubakar Sidick
Wilfried Sewadé
Come Zinsou Koukpo
Saïd Chitou
Linda Towakinou
Bruno Adjottin
Steve Hougbe
Filémon Tokponnon
Germain Gil Padonou
Martin Akogbéto
Louisa A. Messenger
Razaki A. Ossè
author_facet Minassou Juvénal Ahouandjinou
Arthur Sovi
Aboubakar Sidick
Wilfried Sewadé
Come Zinsou Koukpo
Saïd Chitou
Linda Towakinou
Bruno Adjottin
Steve Hougbe
Filémon Tokponnon
Germain Gil Padonou
Martin Akogbéto
Louisa A. Messenger
Razaki A. Ossè
author_sort Minassou Juvénal Ahouandjinou
collection DOAJ
description Abstract Background Recently, bacterial endosymbiont, including Wolbachia and Microsporidia were found to limit the infection of Anopheles mosquitoes with Plasmodium falciparum. This study aimed to investigate the natural presence of key transmission-blocking endosymbionts in Anopheles gambiae and Anopheles coluzzii in Southern Benin. Methods The present study was conducted in seven communes (Cotonou, Porto-Novo, Aguégués, Ifangni, Pobè Athiémé, and Grand-Popo) of Southern Benin. Anopheles were collected using indoor/outdoor Human Landing Catches (HLCs) and Pyrethrum Spray Catches (PSCs). Following morphological identification, PCR was used to identify An. gambiae sensu lato (s.l.) to species level and to screen for the presence of both Wolbachia and Microsporidia. Plasmodium falciparum sporozoite infection was also assessed using ELISA. Results Overall, species composition in An. gambiae s.l. was 53.7% An. coluzzii, while the remainder was An. gambiae sensu stricto (s.s.). Combined data of the two sampling techniques revealed a mean infection prevalence with Wolbachia of 5.1% (95% CI 0.90–18.6) and 1.3% (95% CI 0.07–7.8) in An. gambiae s.s. and An. coluzzii, respectively. The mean infection prevalence with Microsporidia was 41.0% (95% CI 25.9–57.8) for An. gambiae s.s. and 57.0% (95% CI 45.4–67.9) for An. coluzzii. Wolbachia was only observed in Ifangni, Pobè, and Cotonou, while Microsporidia was detected in all study communes. Aggregated data for HLCs and PSCs showed a sporozoite rate (SR) of 0.80% (95% CI 0.09–2.87) and 0.69% (95% CI 0.09–2.87) for An. gambiae and An. coluzzii, respectively, with a mean of 0.74% (95% CI 0.20–1.90). Of the four individual mosquitoes which harboured P. falciparum, none were also infected with Wolbachia and one contained Microsporidia. Conclusions The present study is the first report of natural infections of field-collected An. gambiae s.l. populations from Benin with Wolbachia and Microsporidia. Sustained efforts should be made to widen the spectrum of bacteria identified in mosquitoes, with the potential to develop endosymbiont-based control tools; such interventions could be the game-changer in the control of malaria and arboviral disease transmission.
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spelling doaj.art-4ffa041370b34084b60184569644ed0a2024-03-17T12:16:10ZengBMCMalaria Journal1475-28752024-03-012311910.1186/s12936-024-04906-1First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional studyMinassou Juvénal Ahouandjinou0Arthur Sovi1Aboubakar Sidick2Wilfried Sewadé3Come Zinsou Koukpo4Saïd Chitou5Linda Towakinou6Bruno Adjottin7Steve Hougbe8Filémon Tokponnon9Germain Gil Padonou10Martin Akogbéto11Louisa A. Messenger12Razaki A. Ossè13Centre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouBiology Department, VERG Laboratories, Hacettepe UniversityCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouCentre de Recherche Entomologique de CotonouDisease Control Department, Faculty of Infectious and Tropical Diseases, London School of Hygiene and Tropical MedicineCentre de Recherche Entomologique de CotonouAbstract Background Recently, bacterial endosymbiont, including Wolbachia and Microsporidia were found to limit the infection of Anopheles mosquitoes with Plasmodium falciparum. This study aimed to investigate the natural presence of key transmission-blocking endosymbionts in Anopheles gambiae and Anopheles coluzzii in Southern Benin. Methods The present study was conducted in seven communes (Cotonou, Porto-Novo, Aguégués, Ifangni, Pobè Athiémé, and Grand-Popo) of Southern Benin. Anopheles were collected using indoor/outdoor Human Landing Catches (HLCs) and Pyrethrum Spray Catches (PSCs). Following morphological identification, PCR was used to identify An. gambiae sensu lato (s.l.) to species level and to screen for the presence of both Wolbachia and Microsporidia. Plasmodium falciparum sporozoite infection was also assessed using ELISA. Results Overall, species composition in An. gambiae s.l. was 53.7% An. coluzzii, while the remainder was An. gambiae sensu stricto (s.s.). Combined data of the two sampling techniques revealed a mean infection prevalence with Wolbachia of 5.1% (95% CI 0.90–18.6) and 1.3% (95% CI 0.07–7.8) in An. gambiae s.s. and An. coluzzii, respectively. The mean infection prevalence with Microsporidia was 41.0% (95% CI 25.9–57.8) for An. gambiae s.s. and 57.0% (95% CI 45.4–67.9) for An. coluzzii. Wolbachia was only observed in Ifangni, Pobè, and Cotonou, while Microsporidia was detected in all study communes. Aggregated data for HLCs and PSCs showed a sporozoite rate (SR) of 0.80% (95% CI 0.09–2.87) and 0.69% (95% CI 0.09–2.87) for An. gambiae and An. coluzzii, respectively, with a mean of 0.74% (95% CI 0.20–1.90). Of the four individual mosquitoes which harboured P. falciparum, none were also infected with Wolbachia and one contained Microsporidia. Conclusions The present study is the first report of natural infections of field-collected An. gambiae s.l. populations from Benin with Wolbachia and Microsporidia. Sustained efforts should be made to widen the spectrum of bacteria identified in mosquitoes, with the potential to develop endosymbiont-based control tools; such interventions could be the game-changer in the control of malaria and arboviral disease transmission.https://doi.org/10.1186/s12936-024-04906-1WolbachiaMicrosporidiaAnopheles coluzziiAnopheles gambiae
spellingShingle Minassou Juvénal Ahouandjinou
Arthur Sovi
Aboubakar Sidick
Wilfried Sewadé
Come Zinsou Koukpo
Saïd Chitou
Linda Towakinou
Bruno Adjottin
Steve Hougbe
Filémon Tokponnon
Germain Gil Padonou
Martin Akogbéto
Louisa A. Messenger
Razaki A. Ossè
First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional study
Malaria Journal
Wolbachia
Microsporidia
Anopheles coluzzii
Anopheles gambiae
title First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional study
title_full First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional study
title_fullStr First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional study
title_full_unstemmed First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional study
title_short First report of natural infection of Anopheles gambiae s.s. and Anopheles coluzzii by Wolbachia and Microsporidia in Benin: a cross-sectional study
title_sort first report of natural infection of anopheles gambiae s s and anopheles coluzzii by wolbachia and microsporidia in benin a cross sectional study
topic Wolbachia
Microsporidia
Anopheles coluzzii
Anopheles gambiae
url https://doi.org/10.1186/s12936-024-04906-1
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