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

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.