Extensive circadian and light regulation of the transcriptome in the malaria mosquito Anopheles gambiae

Abstract

BackgroundMosquitoes exhibit 24 hr rhythms in flight activity, feeding, reproduction and development. To better understand the molecular basis for these rhythms in the nocturnal malaria vector Anopheles gambiae, we have utilized microarray analysis on time-of-day specific collections of mosquitoes over 48 hr to explore the coregulation of gene expression rhythms by the circadian clock and light, and compare these with the 24 hr rhythmic gene expression in the diurnal Aedes aegypti dengue vector mosquito.ResultsIn time courses from An. gambiae head and body collected under light:dark cycle (LD) and constant dark (DD) conditions, we applied three algorithms that detect sinusoidal patterns and an algorithm that detects spikes in expression. This revealed across four experimental conditions 393 probes newly scored as rhythmic. These genes correspond to functions such as metabolic detoxification, immunity and nutrient sensing. This includes glutathione S-transferase GSTE5, whose expression pattern and chromosomal location are shared with other genes, suggesting shared chromosomal regulation; and pulsatile expression of the gene encoding CYP6M2, a cytochrome P450 that metabolizes pyrethroid insecticides. We explored the interaction of light and the circadian clock and highlight the regulation of odorant binding proteins (OBPs), important components of the olfactory system. We reveal that OBPs have unique expression patterns as mosquitoes make the transition from LD to DD conditions. We compared rhythmic expression between An. gambiae and Ae. aegypti heads collected under LD conditions using a single cosine fitting algorithm, and report distinct similarities and differences in the temporal regulation of genes involved in tRNA priming, the vesicular-type ATPase, olfaction and vision between the two species.ConclusionsThese data build on our previous analyses of time-of-day specific regulation of the An. gambiae transcriptome to reveal additional rhythmic genes, an improved understanding of the co-regulation of rhythms in gene expression by the circadian clock and by light, and an understanding of the time-of-day specific regulation of some of these rhythmic processes in comparison with a different species of mosquito. Improved understanding of biological timing at the molecular level that underlies key physiological aspects of mosquito vectors may prove to be important to successful implementation of established and novel insect control methods.

The transcriptome of the mosquito Aedes fluviatilis (Diptera: Culicidae), and transcriptional changes associated with its native Wolbachia infection

“…There have been no categorised effects of Wolbachia on host visual process, and no similar genes were affected by w Mel or w MelPop [11]. Potential physiological consequences of these changes could be a decreased sensitivity to light, which would be disadvantageous to the mosquito, or may indicate decreased activity during low level light conditions [88–90]. …”

OUP accepted manuscript

“…Because more and more cycling genes have been identified, the collection and integration of the data is helpful for further experimental consideration. Previously, four major databases were developed for circadian genes, including DIURNAL (23), CircaDB (29), SCNseq (30) and Bioclock (31–33). The DIURNAL database maintains circadian microarray data for three plants, including Arabidopsis thaliana , poplar and rice (23).…”

“…CircaDB contains over 3000 potential circadian genes in human and mouse (29). SCNseq contains 4569 cycling genes, and 3187 intergenic non-coding RNAs in mice, whereas Bioclock contains 1674 potential circadian genes exclusively in Aedes aegypti and ∼1000 potential circadian genes in Anopheles gambiae (31–33). Although a number of computational efforts have been contributed to this area, an integrative resource is still not available.…”

Transcriptome analysis of molecular mechanisms responsible for light-stress response in Mythimna separata (Walker)

“…However, understanding of the molecular responses of insects to light is based on a small number of species373839404142, and has mainly focused on two pathways of circadian rhythm and phototransduction. Several genes related to circadian rhythm have been identified in Drosophila melanogaster 16, Anopheles gambiae 37 and Ptomaphagus hirtus 38, and genes related to phototransduction have been found in D. melanogaster 394041 and Periplaneta americana 42.…”