A comprehensive transcriptomic view of renal function in the malaria vector, Anopheles gambiae

Abstract

Renal function is essential to maintain homeostasis. This is particularly significant for insects that undergo complete metamorphosis; larval mosquitoes must survive a freshwater habitat whereas adults are terrestrial, and mature females must maintain ion and fluid homeostasis after blood feeding. To investigate the physiological adaptations required for successful development to adulthood, we studied the Malpighian tubule transcriptome of Anopheles gambiae using Affymetrix arrays. We assessed transcription under several conditions; as third instar larvae, as adult males fed on sugar, as adult females fed on sugar, and adult females after a blood meal. In addition to providing the most detailed transcriptomic data to date on the Anopheles Malpighian tubules, the data provide unique information on the renal adaptations required for the switch from freshwater to terrestrial habitats, on gender differences, and on the contrast between nectar-feeding and haematophagy. We found clear differences associated with ontogenetic change in lifestyle, gender and diet, particularly in the neuropeptide receptors that control fluid secretion, and the water and ion transporters that impact volume and composition. These data were also combined with transcriptomics from the Drosophila melanogaster tubule, allowing meta-analysis of the genes which underpin tubule function across Diptera. To further investigate renal conservation across species we selected four Drosophila melanogaster genes with orthologues highly enriched in the Anopheles tubules, and generated RNAi knockdown flies. Three of these genes proved essential, showing conservation of critical functions across 150 million years of phylogenetic separation. This extensive data-set is available as an online resource, MozTubules.org, and could potentially be mined for novel insecticide targets that can impact this critical organ in this pest species.

RNA-Seq Comparison of Larval and Adult Malpighian Tubules of the Yellow Fever Mosquito Aedes aegypti Reveals Life Stage-Specific Changes in Renal Function

“…This is in contrast to microarray data from A. gambiae which indicates that in this mosquito species V-ATPase subunits are generally higher expressed in adults compared to larvae (Overend et al, 2015). …”

“…An ortholog of this transcript was also highly abundant in the MT of adult female A. albopictus and A. gambiae (Overend et al, 2015; Esquivel et al, 2016). NCKX1 may be associated with the response of MTs to kinins.…”

“…Previous studies have characterized the transcriptome of the MT in A. albopictus (before and after blood feeding) (Esquivel et al, 2014, 2016) and A. gambiae (larval, adult, before, and after blood feeding) (Overend et al, 2015), but transcriptomic studies in the MT of A. aegypti have not previously been performed. The goal of this study was to characterize the changes occurring in the MT of A. aegypti mosquitoes when switching from an aquatic to a terrestrial life.…”

Malpighian Tubules as Novel Targets for Mosquito Control

“…Notably, in the Malpighian tubules of An. gambiae , a transcript for kynurenine 3-monoxygenase was also highly enriched at 3 h post-blood meal [29]. These findings suggest that the Malpighian tubules contribute to antioxidant production and heme detoxification in mosquitoes during blood meal processing.…”

RNA Interference for Mosquito and Mosquito-Borne Disease Control

“…aegypti [101]. Overend et al (2015) state the importance of diuresis with “genes that show conservation…in the Malpighian tubules of Anopheles and Drosophila are likely to be essential for survival” [102]. Indeed, RNAi induced suppression of diuresis via aquaporin suppression increases fluid retention resulting in mosquito tolerance to desiccation improving survival under stress [103,104].…”