Molecular, biochemical, and physiological evidence for a functional transition in the 'kidneys' of adult female mosquitoes during the processing of blood meals

The insect analogs of mammalian kidneys are Malpighian tubules.  In adult female mosquitoes, the Malpighian tubules mediate a diuresis that starts when engorging on the blood of a vertebrate host and lasts for ~2 h.  The diuresis rids the mosquito of the unwanted salt and water that are absorbed into the hemolymph.  Once the diuresis subsides, the contributions that the Malpighian tubules make towards the processing of blood meals are not well understood.  To address this gap of knowledge we used RNA-Seq to characterize the transcriptomes of Malpighian tubules in adult female Asian tiger mosquitoes (Aedes albopictus) under non-blood fed and blood fed (3-24 h after ingestion) conditions.  We found that the Malpighian tubules of non-blood fed mosquitoes express mRNAs encoding proteins involved with 1) transepithelial fluid secretion (i.e., diuresis), and 2) redox/detoxification mechanisms (e.g., thioredoxin).  After blood feeding, we found concerted 1) accumulations of mRNAs encoding proteins associated with redox and detoxification mechanisms (e.g., glutathione S-transferases, thioredoxin, xanthine dehydrogenase, ABC transporters), and 2) reductions of mRNAs encoding proteins associated with diuresis (e.g., subunits of the V-type H⁺-ATPase, aquaporins, ion channels/transporters).  Assays to measure the activity of glutathione S-transferase and the content of uric acid in isolated Malpighian tubules confirm a biochemical increase of detoxification mechanisms after blood feeding.  Furthermore, assays to measure the diuretic capacity of intact mosquitoes confirm a reduced physiological capability of mosquitoes to excrete urine after blood feeding.  Our results provide new insights into the roles of mosquito ‘kidneys’ in the processing of blood meals.