Novel insights into the metabolic and biochemical underpinnings assisting dry-season survival in female malaria mosquitoes of the Anopheles gambiae complex

Schematic resume of the different physiological and biochemical assays performed in both M and S forms of An. gambiae following developmental acclimation to rainy season (“rs”) and onset of the dry season (“ods”) conditions. [Display omitted] •We examined the desiccation tolerance in 1-h- and 24-h-old female An. gambiae s.s.•Phe, tyr, and val involved in cuticle permeability decreased after the emergence.•Metabolomic and proteomic data suggest changes in cuticle composition in the M form.•Increased expression of TCA cycle enzymes suggest higher metabolic rate in the S form. The mechanisms by which Anopheles gambiae mosquitoes survive the desiccating conditions of the dry season in Africa and are able to readily transmit malaria soon after the rains start remain largely unknown. The desiccation tolerance and resistance of female An. gambiae M and S reared in contrasting environmental conditions reflecting the onset of dry season (“ods”) and the rainy season (“rs”) was determined by monitoring their survival and body water loss in response to low relative humidity. Furthermore, we investigated the degree to which the physiology of 1-h and 24-h-old females is altered at “ods” by examining and comparing their quantitative metabotypes and proteotypes with conspecifics exposed to “rs” conditions. Results showed that distinct biochemical rearrangements occurred soon after emergence in female mosquitoes that enhance survival and limit water loss under dry conditions. In particular, three amino acids (phenylalanine, tyrosine, and valine) playing a pivotal role in cuticle permeability decreased significantly from the 1-h to 24-h-old females, regardless of the experimental conditions. However, these amino acids were present in higher amounts in 1-h-old female An. gambiae M reared under “ods” whereas no such seasonal difference was reported in S ones. Together with the 1.28- to 2.84-fold increased expression of cuticular proteins 70 and 117, our data suggests that cuticle composition, rigidity and permeability were adjusted at “ods”. Increased expression of enzymes involved in glycogenolytic and proteolytic processes were found in both forms at “ods”. Moreover, 1-h-old S forms were characterised by elevated amounts of glycogen phosphorylase, isocitrate dehydrogenase, and citrate synthase, suggesting an increase of energetic demand in these females at “ods”.