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

Abstract

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".

Comparative physiological plasticity to desiccation in distinct populations of the malarial mosquito Anopheles coluzzii

“…Increased body water amount was demonstrated to be the primary mechanism enhancing desiccation resistance in flies [38, 39], and this response was also observed in newly emerged An. coluzzii females [16]. Meanwhile, in the present study, body water content and dynamics of body water loss remained similar between RS- and ODS-reared females from their emergence, and until they were aged of 7 days.…”

“…A previous study showed that hexamerin A and 2β were characterised by drastic reductions at ODS in An. coluzzii females [16]. Then, amino acids resulting from the breakdown of proteins could fuel the energetic metabolism [40], and/or could be used as substrates for the synthesis of metabolites with osmoprotective functions [7, 41].…”

“…This ability of An. coluzzii to endure a large range of temperature and relative humidity conditions across their larval ecotypes likely results from their capacity to express several distinct phenotypes [16], explaining, at least partially, the robustness of malaria transmission throughout West Africa from one season to the next. Consistently, at the onset of the dry season, it was established that female An.…”

Metabolic adaptations in a range‐expanding arthropod

“…; Hidalgo et al. ). It provides information on the interaction between an organism's physiology and its natural environment by identifying metabolites of low‐to‐moderate molecular mass within the whole body, cells, tissues, or biofluids.…”

“…Metabolomics is a convenient technique which can be used as a candidate approach to explore an organism's response to environmental variations and forthcoming environmental changes (Hines et al 2007;Miller 2007;Viant 2008;Bundy et al 2009;Lankadurai et al 2013;Hidalgo et al 2014). It provides information on the interaction between an organism's physiology and its natural environment by identifying metabolites of low-to-moderate molecular mass within the whole body, cells, tissues, or biofluids.…”