Spatial and sex-specific dissection of the Anopheles gambiae midgut transcriptome

Emma Warr,Vassiliki Mahairaki,Ruth Aguilar,Yuemei Dong,George Dimopoulos

doi:10.1186/1471-2164-8-37

Abstract

BackgroundThe midgut of hematophagous insects, such as disease transmitting mosquitoes, carries out a variety of essential functions that mostly relate to blood feeding. The midgut of the female malaria vector mosquito Anopheles gambiae is a major site of interactions between the parasite and the vector. Distinct compartments and cell types of the midgut tissue carry out specific functions and vector borne pathogens interact and infect different parts of the midgut.ResultsA microarray based global gene expression approach was used to compare transcript abundance in the four major female midgut compartments (cardia, anterior, anterior part of posterior and posterior part of posterior midgut) and between the male and female Anopheles gambiae midgut. Major differences between the female and male midgut gene expression relate to digestive processes and immunity. Each compartment has a distinct gene function profile with the posterior midgut expressing digestive enzyme genes and the cardia and anterior midgut expressing high levels of antimicrobial peptide and other immune gene transcripts. Interestingly, the cardia expressed several known anti-Plasmodium factors. A parallel peptidomic analysis of the cardia identified known mosquito antimicrobial peptides as well as several putative short secreted peptides that are likely to represent novel antimicrobial factors.ConclusionThe A. gambiae sex specific midgut and female midgut compartment specific transcriptomes correlates with their known functions. The significantly greater functional diversity of the female midgut relate to hematophagy that is associated with digestion and nutrition uptake as well as exposes it to a variety of pathogens, and promotes growth of its endogenous microbial flora. The strikingly high proportion of immunity related factors in the cardia tissue most likely serves the function to increase sterility of ingested sugar and blood. A detailed characterization of the functional specificities of the female mosquito midgut and its various compartments can greatly contribute to our understanding of its role in disease transmission and generate the necessary tools for the development of malaria control strategies.

Highlights

The midgut of hematophagous insects, such as disease transmitting mosquitoes, carries out a variety of essential functions that mostly relate to blood feeding
Female mosquitoes are capable of transmitting a variety of pathogens and as such the midgut has become an important focus for studies that aim at understanding the transmission biology of vector-borne diseases [1,2,3,4,5,6,7,8,9,10]
In addition to their essential role in blood-meal digestion, trypsins have been shown to be required for the activation of an ookinete-secreted chitinase, which enables the parasite to penetrate the peritrophic matrix of the mosquito midgut [20,21,22]

Summary

Introduction

The midgut of hematophagous insects, such as disease transmitting mosquitoes, carries out a variety of essential functions that mostly relate to blood feeding. A variety of studies, including microarray-based gene expression analyses, have addressed the effect of infection or blood-meal ingestion on the female mosquito These studies have established the immune responsive capacity of the midgut and provide detailed information about a variety of biological processes that are regulated upon blood feeding [1,2,3,5,6,7,8,9,10,11,12]. Regenerative and endocrine cells are present in the posterior midgut, their function is currently unknown [14] In addition to their essential role in blood-meal digestion, trypsins have been shown to be required for the activation of an ookinete-secreted chitinase, which enables the parasite to penetrate the peritrophic matrix of the mosquito midgut [20,21,22]. A variety of transporters responsible for maintaining osmotic balance and nutritient uptake are expressed in the midgut and are regulated upon feeding [9]

Methods

Results

Conclusion