Abstract

Hematophagous mosquitoes serve as vectors of multiple devastating human diseases, and many unique physiological features contribute to the incredible evolutionary success of these insects. These functions place high-energy demands on a reproducing female mosquito, and carbohydrate metabolism (CM) must be synchronized with these needs. Functional analysis of metabolic gene profiling showed that major CM pathways, including glycolysis, glycogen and sugar metabolism, and citrate cycle, are dramatically repressed at post eclosion (PE) stage in mosquito fat body followed by a sharply increase at post-blood meal (PBM) stage, which were also verified by Real-time RT-PCR. Consistent to the change of transcript and protein level of CM genes, the level of glycogen, glucose and trehalose and other secondary metabolites are also periodically accumulated and degraded during the reproductive cycle respectively. Levels of triacylglycerols (TAG), which represent another important energy storage form in the mosquito fat body, followed a similar tendency. On the other hand, ATP, which is generated by catabolism of these secondary metabolites, showed an opposite trend. Additionally, we used RNA interference studies for the juvenile hormone and ecdysone receptors, Met and EcR, coupled with transcriptomics and metabolomics analyses to show that these hormone receptors function as major regulatory switches coordinating CM with the differing energy requirements of the female mosquito throughout its reproductive cycle. Our study demonstrates how, by metabolic reprogramming, a multicellular organism adapts to drastic and rapid functional changes.

Highlights

  • The ability of multicellular organisms to maintain metabolic homeostasis and respond to changing energy requirements during development, reproduction and stress represents an essential adaptation critical for survival and evolutionary success

  • Metabolism must be synchronized with high energetic needs of a female mosquito for host seeking, blood feeding and rapid egg development

  • Each reproductive cycle is divided into two phases that are sequentially governed by juvenile hormone (JH) and 20-hydroxyecdysone

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Summary

Introduction

The ability of multicellular organisms to maintain metabolic homeostasis and respond to changing energy requirements during development, reproduction and stress represents an essential adaptation critical for survival and evolutionary success. It is important to decipher regulatory mechanisms coordinating metabolic pathways; understanding these mechanisms in organisms facing extreme and fluctuating energy demands is valuable. Female mosquitoes, which are obligatory blood feeders, serve as disease vectors [1]. Pathogens, taking advantage of this blood dependency, use mosquitoes as vectors spreading serious human diseases. Despite continuing efforts and advances in insect control, mosquitoes pose an enormous threat, killing over a million people each year. A detailed understanding of the reproductive biology of the mosquito may provide vital information to take us a step closer to more effective vector-control strategies

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