Aedes aegypti post-emergence transcriptome: Unveiling the molecular basis for the hematophagic and gonotrophic capacitation

Author summary Aedes aegypti is a vector of several human diseases such as Dengue, Zika, Chikungunya, and Yellow Fever. Only the adult females can feed on blood, important for the production of their offspring, and therefore transmitting these pathogens for the human host. Interestingly, right after their emergence as adults, females show a preference of feeding on nectar, and only after three days, they are fully capacitated to perform a blood meal. Understanding the molecular mechanisms that orchestrate this physiological and biochemical switch is the main topic of the present study. The transcriptome analysis of males and females during the first hours post-emergence reveals that the gene expression in females is tightly regulated, showing three time-dependent profiles of expression. There is an increase in genes related to the oxidative phosphorylation pathway in the female head. Assessment of mitochondrial function revealed a gradual increase in respiration linked to ATP synthesis and mitochondrial content. Also, there is an increase in genes related to the muscular function, suggesting a putative role in muscle development and contraction, required, for example, for pumping of blood. The female body showed an increase in salivary gland related genes and serine proteases, probably related to the ingestion and digestion of the blood. Also, the increase in DNA replication, ribosome biogenesis, and juvenile hormone signaling pathways together with changes in cell cycle control suggest the gonotrophic capacitation for the massive synthesis of yolk proteins precursors during vitellogenesis. All these genes were enhanced even before the first blood meal, which reveals insightful information about the biology of anautogenous mosquitoes. Our data showed the molecular machinery that stands the females hematophagy and gonotrophy, leading to potential new targets for vector control. The adult females of Aedes aegypti mosquitoes are facultative hematophagous insects but they are unable to feed on blood right after pupae emergence. The maturation process that takes place during the first post-emergence days, hereafter named hematophagic and gonotrophic capacitation, comprises a set of molecular and physiological changes that prepare the females for the first gonotrophic cycle. Notwithstanding, the molecular bases underlying mosquito hematophagic and gonotrophic capacitation remain obscure. Here, we investigated the molecular and biochemical changes in adult Ae. aegypti along the first four days post-emergence, prior to a blood meal. We performed a RNA-Seq analysis of the head and body, comparing male and female gene expression time courses. A total of 811 and 203 genes were differentially expressed, respectively in the body and head, and both body parts showed early, mid, and late female-specific expression profiles. Female-specific up-regulation of genes involved in muscle development and the oxidative phosphorylation pathway were remarkable features observed in the head. Functional assessment of mitochondrial oxygen consumption in heads showed a gradual increase in respiratory capacity and ATP-linked respiration as a consequence of induced mitochondrial biogenesis and content over time. This pattern strongly suggests that boosting oxidative phosphorylation in heads is a required step towards blood sucking habit. Several salivary gland genes, proteases, and genes involved in DNA replication and repair, ribosome biogenesis, and juvenile hormone signaling were up-regulated specifically in the female body, which may reflect the gonotrophic capacitation. This comprehensive description of molecular and biochemical mechanisms of the hematophagic and gonotrophic capacitation in mosquitoes unravels potentially new targets for vector control.

Automated summary

The author's study focused on understanding the molecular mechanisms behind the feeding behavior of Aedes aegypti mosquitoes, particularly the transition from nectar feeding to blood feeding in adult females. Through transcriptome analysis, it was found that genes related to oxidative phosphorylation, muscle development, salivary gland function, and DNA replication were up-regulated in females post-emergence. This study provides insights into the physiological and biochemical changes that prepare female mosquitoes for blood feeding, offering potential new targets for vector control.