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Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi

Blood-feeding enriched gut-microbiota boosts mosquitoes' anti-Plasmodium immunity. Here, we ask how Plasmodium vivax alters gut-microbiota, anti-Plasmodial immunity, and impacts tripartite Plasmodium-mosquito-microbiota interactions in the gut lumen. We used a metagenomics and RNAseq strategy t...

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Autores principales: Sharma, Punita, Rani, Jyoti, Chauhan, Charu, Kumari, Seena, Tevatiya, Sanjay, Das De, Tanwee, Savargaonkar, Deepali, Pandey, Kailash C., Dixit, Rajnikant
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7240202/
https://www.ncbi.nlm.nih.gov/pubmed/32477320
http://dx.doi.org/10.3389/fimmu.2020.00609
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author Sharma, Punita
Rani, Jyoti
Chauhan, Charu
Kumari, Seena
Tevatiya, Sanjay
Das De, Tanwee
Savargaonkar, Deepali
Pandey, Kailash C.
Dixit, Rajnikant
author_facet Sharma, Punita
Rani, Jyoti
Chauhan, Charu
Kumari, Seena
Tevatiya, Sanjay
Das De, Tanwee
Savargaonkar, Deepali
Pandey, Kailash C.
Dixit, Rajnikant
author_sort Sharma, Punita
collection PubMed
description Blood-feeding enriched gut-microbiota boosts mosquitoes' anti-Plasmodium immunity. Here, we ask how Plasmodium vivax alters gut-microbiota, anti-Plasmodial immunity, and impacts tripartite Plasmodium-mosquito-microbiota interactions in the gut lumen. We used a metagenomics and RNAseq strategy to address these questions. In naïve mosquitoes, Elizabethkingia meningitis and Pseudomonas spp. are the dominant bacteria and blood-feeding leads to a heightened detection of Elizabethkingia, Pseudomonas and Serratia 16S rRNA. A parallel RNAseq analysis of blood-fed midguts also shows the presence of Elizabethkingia-related transcripts. After, P. vivax infected blood-meal, however, we do not detect bacterial 16S rRNA until circa 36 h. Intriguingly, the transcriptional expression of a selected array of antimicrobial arsenal cecropins 1–2, defensin-1, and gambicin remained low during the first 36 h—a time frame when ookinetes/early oocysts invaded the gut. We conclude during the preinvasive phase, P. vivax outcompetes midgut-microbiota. This microbial suppression likely negates the impact of mosquito immunity which in turn may enhance the survival of P. vivax. Detection of sequences matching to mosquito-associated Wolbachia opens a new inquiry for its exploration as an agent for “paratransgenesis-based” mosquito control.
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spelling pubmed-72402022020-05-29 Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi Sharma, Punita Rani, Jyoti Chauhan, Charu Kumari, Seena Tevatiya, Sanjay Das De, Tanwee Savargaonkar, Deepali Pandey, Kailash C. Dixit, Rajnikant Front Immunol Immunology Blood-feeding enriched gut-microbiota boosts mosquitoes' anti-Plasmodium immunity. Here, we ask how Plasmodium vivax alters gut-microbiota, anti-Plasmodial immunity, and impacts tripartite Plasmodium-mosquito-microbiota interactions in the gut lumen. We used a metagenomics and RNAseq strategy to address these questions. In naïve mosquitoes, Elizabethkingia meningitis and Pseudomonas spp. are the dominant bacteria and blood-feeding leads to a heightened detection of Elizabethkingia, Pseudomonas and Serratia 16S rRNA. A parallel RNAseq analysis of blood-fed midguts also shows the presence of Elizabethkingia-related transcripts. After, P. vivax infected blood-meal, however, we do not detect bacterial 16S rRNA until circa 36 h. Intriguingly, the transcriptional expression of a selected array of antimicrobial arsenal cecropins 1–2, defensin-1, and gambicin remained low during the first 36 h—a time frame when ookinetes/early oocysts invaded the gut. We conclude during the preinvasive phase, P. vivax outcompetes midgut-microbiota. This microbial suppression likely negates the impact of mosquito immunity which in turn may enhance the survival of P. vivax. Detection of sequences matching to mosquito-associated Wolbachia opens a new inquiry for its exploration as an agent for “paratransgenesis-based” mosquito control. Frontiers Media S.A. 2020-05-14 /pmc/articles/PMC7240202/ /pubmed/32477320 http://dx.doi.org/10.3389/fimmu.2020.00609 Text en Copyright © 2020 Sharma, Rani, Chauhan, Kumari, Tevatiya, Das De, Savargaonkar, Pandey and Dixit. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Immunology
Sharma, Punita
Rani, Jyoti
Chauhan, Charu
Kumari, Seena
Tevatiya, Sanjay
Das De, Tanwee
Savargaonkar, Deepali
Pandey, Kailash C.
Dixit, Rajnikant
Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi
title Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi
title_full Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi
title_fullStr Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi
title_full_unstemmed Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi
title_short Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi
title_sort altered gut microbiota and immunity defines plasmodium vivax survival in anopheles stephensi
topic Immunology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7240202/
https://www.ncbi.nlm.nih.gov/pubmed/32477320
http://dx.doi.org/10.3389/fimmu.2020.00609
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