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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doaj-c99f2e0ace5b4620890a87681f69c7bf2020-11-25T02:57:27ZengFrontiers Media S.A.Frontiers in Immunology1664-32242020-05-011110.3389/fimmu.2020.00609513192Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensiPunita Sharma0Jyoti Rani1Jyoti Rani2Charu Chauhan3Seena Kumari4Sanjay Tevatiya5Tanwee Das De6Deepali Savargaonkar7Kailash C. Pandey8Rajnikant Dixit9Laboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaBio and Nanotechnology Department, Guru Jambheshwar University of Science and Technology, Haryana, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaLaboratory of Host-Parasite Interaction Studies, ICMR-National Institute of Malaria Research, New Delhi, IndiaBlood-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.https://www.frontiersin.org/article/10.3389/fimmu.2020.00609/fullAnopheles stephensimidgutmicrobiomePlasmodium vivaxtripartite interactions |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Punita Sharma Jyoti Rani Jyoti Rani Charu Chauhan Seena Kumari Sanjay Tevatiya Tanwee Das De Deepali Savargaonkar Kailash C. Pandey Rajnikant Dixit |
spellingShingle |
Punita Sharma Jyoti Rani Jyoti Rani Charu Chauhan Seena Kumari Sanjay Tevatiya Tanwee Das De Deepali Savargaonkar Kailash C. Pandey Rajnikant Dixit Altered Gut Microbiota and Immunity Defines Plasmodium vivax Survival in Anopheles stephensi Frontiers in Immunology Anopheles stephensi midgut microbiome Plasmodium vivax tripartite interactions |
author_facet |
Punita Sharma Jyoti Rani Jyoti Rani Charu Chauhan Seena Kumari Sanjay Tevatiya Tanwee Das De Deepali Savargaonkar Kailash C. Pandey Rajnikant Dixit |
author_sort |
Punita Sharma |
title |
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_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_sort |
altered gut microbiota and immunity defines plasmodium vivax survival in anopheles stephensi |
publisher |
Frontiers Media S.A. |
series |
Frontiers in Immunology |
issn |
1664-3224 |
publishDate |
2020-05-01 |
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. |
topic |
Anopheles stephensi midgut microbiome Plasmodium vivax tripartite interactions |
url |
https://www.frontiersin.org/article/10.3389/fimmu.2020.00609/full |
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