Abstract
The blood meal of the female malaria mosquito is a pre-requisite to egg production and also represents the transmission route for the malaria parasite. The proper and rapid assimilation of proteins and nutrients in the blood meal creates a significant metabolic challenge for the mosquito. To better understand this process we generated a global profile of metabolite changes in response to blood meal of Anopheles gambiae, using Gas Chromatography-Mass Spectrometry (GC-MS). To disrupt a key pathway of amino acid metabolism we silenced the gene phenylalanine hydroxylase (PAH) involved in the conversion of the amino acid phenylalanine into tyrosine. We observed increased levels of phenylalanine and the potentially toxic metabolites phenylpyruvate and phenyllactate as well as a reduction in the amount of tyrosine available for melanin synthesis. This in turn resulted in a significant impairment of the melanotic encapsulation response against the rodent malaria parasite Plasmodium berghei. Furthermore silencing of PAH resulted in a significant impairment of mosquito fertility associated with reduction of laid eggs, retarded vitellogenesis and impaired melanisation of the chorion. Carbidopa, an inhibitor of the downstream enzyme DOPA decarboxylase that coverts DOPA into dopamine, produced similar effects on egg melanization and hatching rate suggesting that egg chorion maturation is mainly regulated via dopamine. This study sheds new light on the role of amino acid metabolism in regulating reproduction and immunity.
Highlights
Female Anopheles mosquitoes require a blood meal of their human or animal hosts in order to initiate egg development
At 3 h post-blood meal (PBM) the mRNA was mainly transcribed in the head, carcass and midgut while the highest level of expression was observed in the ovaries at 24 h PBM
The spatial-temporal expression pattern of phenylalanine hydroxylase (PAH) mirrored transcriptional changes associated with blood meal induced metabolic and physiological changes ranging from immunity-related responses involving the fatbody, midgut and hemocytes [22,23], protein digestion in the midgut [24], the synthesis of neuropeptides and hormones in the head [25] and egg development in the ovaries [26]
Summary
Female Anopheles mosquitoes require a blood meal of their human or animal hosts in order to initiate egg development. Repeated blood meals increase the reproductive capacity and make those females efficient disease vectors of malaria by increasing the potential to spread Plasmodium parasites from host to host Because of this tight link between reproduction and disease transmission an understanding of the molecular mechanisms that control the reproduction biology and immunity response of these vectors could elucidate new ways to block parasite transmission. The same PPO enzymes involved in egg hardening have been shown as essential in the innate immune response against a wide range of mosquito pathogens [2,13,14,15,16,17]
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