Abstract
BackgroundThe 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 FindingsHere 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/SignificanceThe 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.
Highlights
The Asian tiger mosquito Aedes albopictus is considered one of the most invasive mosquito species in the world; since 1979 it has spread to over 28 countries outside of its native range in Asia and Southeast Asia, aided by the international trade of used automobile tires [1,2]
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
As explained in the Methods, Malpighian tubules were isolated from mosquitoes at 3 different time points after being fed a blood meal (3 h, 12 h, 24 h)
Summary
The Asian tiger mosquito Aedes albopictus is considered one of the most invasive mosquito species in the world; since 1979 it has spread to over 28 countries outside of its native range in Asia and Southeast Asia, aided by the international trade of used automobile tires [1,2]. Within the United States, the mosquito has spread to at least 36 states and models of its potential for range expansion in the northeastern United States within the few decades are alarming [3] This species is a known or suspected vector of several medically important arboviruses, including chikungunya, dengue, eastern equine encephalitis, La Crosse, West Nile, and yellow fever [4]. 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. It is unclear how the tubules contribute to the metabolism and excretion of wastes (e.g., heme, ammonia) produced during the digestion of blood
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