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

Punita Sharma, Jyoti Rani, Charu Chauhan, Seena Kumari, Sanjay Tevatiya, Tanwee Das De, Deepali Savargaonkar, Kailash C. Pandey, Rajnikant Dixit

2020Frontiers in Immunology66 citationsDOIOpen Access PDF

Abstract

Blood feeding-enriched gut-microbiota boosts mosquitoes’ anti-Plasmodium immunity. Here, we ask how Plasmodium vivax alters gut-microbiota, anti-Plasmodial immunity and impact 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 sps. are the dominant bacteria and blood-feeding leads to heightened detection of Elizabethkingia, Pseudomonas and Serratia 16s RNA. A parallel RNAseq analysis of blood-fed midguts also shows the presence of Elizabethkingia-related transcripts. Post, a Plasmodium vivax infected blood-meal, however, we do not detect bacterial 16sRNA until circa 36 hours. Intriguingly, transcriptional expression of a selected array of antimicrobial arsenal cecropins 1-2, defensin-1 and gambicin remain low during the first 36 hours– a time frame when ookinetes/early oocysts invade gut. We conclude during the preinvasive phase, Plasmodium vivax outcompetes midgut-microbiota. This microbial suppression likely negatively impacts mosquito immunity which in turn may enhance Plasmodium vivax survival. Detection of sequences matching to mosquito-associated Wolbachia opens a new inquiry for its exploration as an agent for ‘paratransgenesis-based’ mosquito control.

Topics & Concepts

Anopheles stephensiPlasmodium vivaxBiologyImmunityMalariaGut floraImmunologyAnophelesImmune systemPlasmodium falciparumEcologyLarvaAedes aegyptiInsect symbiosis and bacterial influencesMosquito-borne diseases and controlGut microbiota and health