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

Abstract

Blood-feeding enriched gut-microbiota boosts mosquitoes' anti-<i>Plasmodium</i> immunity. Here, we ask how <i>Plasmodium vivax</i> alters gut-microbiota, anti-<i>Plasmodial</i> immunity, and impacts tripartite <i>Plasmodium</i>-mosquito-microbiota interactions in the gut lumen. We used a metagenomics and RNAseq strategy to address these questions. In naïve mosquitoes, <i>Elizabethkingia meningitis</i> and <i>Pseudomonas</i> spp. are the dominant bacteria and blood-feeding leads to a heightened detection of <i>Elizabethkingia, Pseudomonas</i> and <i>Serratia 16S rRNA</i>. A parallel RNAseq analysis of blood-fed midguts also shows the presence of <i>Elizabethkingia-related</i> transcripts. After, <i>P. vivax</i> 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, <i>P. vivax</i> outcompetes midgut-microbiota. This microbial suppression likely negates the impact of mosquito immunity which in turn may enhance the survival of <i>P. vivax</i>. Detection of sequences matching to mosquito-associated <i>Wolbachia</i> opens a new inquiry for its exploration as an agent for "paratransgenesis-based" mosquito control.