Transcriptomic Evidence for a Dramatic Functional Transition of the Malpighian Tubules after a Blood Meal in the Asian Tiger Mosquito Aedes albopictus

Abstract

Background

The consumption of a vertebrate blood meal by adult female mosquitoes is necessary for their reproduction, but it also presents significant physiological challenges to mosquito osmoregulation and metabolism. The renal (Malpighian) tubules of mosquitoes play critical roles in the initial processing of the blood meal by excreting excess water and salts that are ingested. However, it is unclear how the tubules contribute to the metabolism and excretion of wastes (e.g., heme, ammonia) produced during the digestion of blood.

Methodology/Principal Findings

Here we used RNA-Seq to examine global changes in transcript expression in the Malpighian tubules of the highly-invasive Asian tiger mosquito Aedes albopictus during the first 24 h after consuming a blood meal. We found progressive, global changes in the transcriptome of the Malpighian tubules isolated from mosquitoes at 3 h, 12 h, and 24 h after a blood meal. Notably, a DAVID functional cluster analysis of the differentially-expressed transcripts revealed 1) a down-regulation of transcripts associated with oxidative metabolism, active transport, and mRNA translation, and 2) an up-regulation of transcripts associated with antioxidants and detoxification, proteolytic activity, amino-acid metabolism, and cytoskeletal dynamics.

Conclusions/Significance

The results suggest that blood feeding elicits a functional transition of the epithelium from one specializing in active transepithelial fluid secretion (e.g., diuresis) to one specializing in detoxification and metabolic waste excretion. Our findings provide the first insights into the putative roles of mosquito Malpighian tubules in the chronic processing of blood meals.

Author Summary

The Asian tiger mosquito Aedes albopictus is a vector of several medically-important arboviruses and one of the most invasive mosquito species in the world. Existing control measures for mosquitoes are presently being challenged by the emergence of resistance to insecticides that target the nervous system. Thus, it is necessary to identify novel physiological targets to guide the development of new insecticides. We recently demonstrated that the ‘kidneys’ (Malpighian tubules) of mosquitoes offer a valuable, new physiological target for insecticides. However, our understanding of how this tissue contributes to the chronic metabolic processing of blood meals by mosquitoes is limited. Here we characterize the changes in transcript expression that occur in the Malpighian tubules of adult female A. albopictus with the goal of identifying key molecular pathways that may reveal valuable targets for insecticide development. We find dramatic changes in transcript accumulation in Malpighian tubules, which 1) provide new insights into the potential functional roles of Malpighian tubules after a blood meal, and 2) reveal new potential molecular pathways and targets to guide the development of new insecticides that would disrupt the renal functions of mosquitoes.