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Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium

During a blood meal, female Anopheles mosquitoes are potentially exposed to diverse microbes in addition to the malaria parasite, Plasmodium. Human and animal African trypanosomiases are frequently co-endemic with malaria in Africa. It is not known whether exposure of Anopheles to trypanosomes influ...

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Autores principales: Dieme, Constentin, Zmarlak, Natalia Marta, Brito-Fravallo, Emma, Travaillé, Christelle, Pain, Adrien, Cherrier, Floriane, Genève, Corinne, Calvo-Alvarez, Estefanía, Riehle, Michelle M., Vernick, Kenneth D., Rotureau, Brice, Mitri, Christian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7032731/
https://www.ncbi.nlm.nih.gov/pubmed/32032359
http://dx.doi.org/10.1371/journal.pntd.0008059
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author Dieme, Constentin
Zmarlak, Natalia Marta
Brito-Fravallo, Emma
Travaillé, Christelle
Pain, Adrien
Cherrier, Floriane
Genève, Corinne
Calvo-Alvarez, Estefanía
Riehle, Michelle M.
Vernick, Kenneth D.
Rotureau, Brice
Mitri, Christian
author_facet Dieme, Constentin
Zmarlak, Natalia Marta
Brito-Fravallo, Emma
Travaillé, Christelle
Pain, Adrien
Cherrier, Floriane
Genève, Corinne
Calvo-Alvarez, Estefanía
Riehle, Michelle M.
Vernick, Kenneth D.
Rotureau, Brice
Mitri, Christian
author_sort Dieme, Constentin
collection PubMed
description During a blood meal, female Anopheles mosquitoes are potentially exposed to diverse microbes in addition to the malaria parasite, Plasmodium. Human and animal African trypanosomiases are frequently co-endemic with malaria in Africa. It is not known whether exposure of Anopheles to trypanosomes influences their fitness or ability to transmit Plasmodium. Using cell and molecular biology approaches, we found that Trypanosoma brucei brucei parasites survive for at least 48h after infectious blood meal in the midgut of the major malaria vector, Anopheles coluzzii before being cleared. This transient survival of trypanosomes in the midgut is correlated with a dysbiosis, an alteration in the abundance of the enteric bacterial flora in Anopheles coluzzii. Using a developmental biology approach, we found that the presence of live trypanosomes in mosquito midguts also reduces their reproductive fitness, as it impairs the viability of laid eggs by affecting their hatching. Furthermore, we found that Anopheles exposure to trypanosomes enhances their vector competence for Plasmodium, as it increases their infection prevalence. A transcriptomic analysis revealed that expression of only two Anopheles immune genes are modulated during trypanosome exposure and that the increased susceptibility to Plasmodium was microbiome-dependent, while the reproductive fitness cost was dependent only on the presence of live trypanosomes but was microbiome independent. Taken together, these results demonstrate multiple effects upon Anopheles vector competence for Plasmodium caused by eukaryotic microbes interacting with the host and its microbiome, which may in turn have implications for malaria control strategies in co-endemic areas.
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spelling pubmed-70327312020-02-28 Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium Dieme, Constentin Zmarlak, Natalia Marta Brito-Fravallo, Emma Travaillé, Christelle Pain, Adrien Cherrier, Floriane Genève, Corinne Calvo-Alvarez, Estefanía Riehle, Michelle M. Vernick, Kenneth D. Rotureau, Brice Mitri, Christian PLoS Negl Trop Dis Research Article During a blood meal, female Anopheles mosquitoes are potentially exposed to diverse microbes in addition to the malaria parasite, Plasmodium. Human and animal African trypanosomiases are frequently co-endemic with malaria in Africa. It is not known whether exposure of Anopheles to trypanosomes influences their fitness or ability to transmit Plasmodium. Using cell and molecular biology approaches, we found that Trypanosoma brucei brucei parasites survive for at least 48h after infectious blood meal in the midgut of the major malaria vector, Anopheles coluzzii before being cleared. This transient survival of trypanosomes in the midgut is correlated with a dysbiosis, an alteration in the abundance of the enteric bacterial flora in Anopheles coluzzii. Using a developmental biology approach, we found that the presence of live trypanosomes in mosquito midguts also reduces their reproductive fitness, as it impairs the viability of laid eggs by affecting their hatching. Furthermore, we found that Anopheles exposure to trypanosomes enhances their vector competence for Plasmodium, as it increases their infection prevalence. A transcriptomic analysis revealed that expression of only two Anopheles immune genes are modulated during trypanosome exposure and that the increased susceptibility to Plasmodium was microbiome-dependent, while the reproductive fitness cost was dependent only on the presence of live trypanosomes but was microbiome independent. Taken together, these results demonstrate multiple effects upon Anopheles vector competence for Plasmodium caused by eukaryotic microbes interacting with the host and its microbiome, which may in turn have implications for malaria control strategies in co-endemic areas. Public Library of Science 2020-02-07 /pmc/articles/PMC7032731/ /pubmed/32032359 http://dx.doi.org/10.1371/journal.pntd.0008059 Text en © 2020 Dieme et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Dieme, Constentin
Zmarlak, Natalia Marta
Brito-Fravallo, Emma
Travaillé, Christelle
Pain, Adrien
Cherrier, Floriane
Genève, Corinne
Calvo-Alvarez, Estefanía
Riehle, Michelle M.
Vernick, Kenneth D.
Rotureau, Brice
Mitri, Christian
Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium
title Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium
title_full Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium
title_fullStr Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium
title_full_unstemmed Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium
title_short Exposure of Anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to Plasmodium
title_sort exposure of anopheles mosquitoes to trypanosomes reduces reproductive fitness and enhances susceptibility to plasmodium
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7032731/
https://www.ncbi.nlm.nih.gov/pubmed/32032359
http://dx.doi.org/10.1371/journal.pntd.0008059
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