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Eggs of the mosquito Aedes aegypti survive desiccation by rewiring their polyamine and lipid metabolism

ABSTRACT: Upon water loss, some organisms pause their life cycles and escape death. While widespread in microbes, this is less common in animals. Aedes mosquitoes are vectors for viral diseases. Aedes eggs can survive dry environments, but molecular and cellular principles enabling egg survival through desiccation remain unknown. In this report, we find that Aedes aegypti eggs, in contrast to Anopheles stephensi, survive desiccation by acquiring desiccation tolerance at a late developmental stage. We uncover unique proteome and metabolic state changes in Aedes embryos during desiccation that reflect reduced central carbon metabolism, rewiring towards polyamine production, and enhanced lipid utilization for energy and polyamine synthesis. Using inhibitors targeting these processes in blood-fed mosquitoes that lay eggs, we infer a two-step process of desiccation tolerance in Aedes eggs. The metabolic rewiring towards lipid breakdown and dependent polyamine accumulation confers resistance to desiccation. Furthermore, rapid lipid breakdown is required to fuel energetic requirements upon water re-entry to enable larval hatching and survival upon rehydration. This study is fundamental to understanding Aedes embryo survival and in controlling the spread of these mosquitoes.

INSTRUMENT(S): Orbitrap Fusion

ORGANISM(S): Aedes Aegypti Aegypti

TISSUE(S): Egg

SUBMITTER: Sreesa Sreedharan

LAB HEAD: Sunil Laxman

PROVIDER: PXD044525 | Pride | 2023-09-26

REPOSITORIES: Pride

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			Action	DRS
	21042021_RID_2717_A1_Rep1.raw	Raw
	21042021_RID_2717_A1_Rep2.raw	Raw
	21042021_RID_2717_A2_Rep1.raw	Raw
	21042021_RID_2717_A2_Rep2.raw	Raw
	21042021_RID_2717_A3_Rep1.raw	Raw

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Project description:Female Aedes aegypti mosquitoes impose a severe global public health burden as primary vectors of multiple viral and parasitic pathogens. Under optimal environmental conditions, Aedes aegypti females have access to human hosts that provide blood proteins for egg development, conspecific males that provide sperm for fertilization, and freshwater that serves as an egg-laying substrate suitable for offspring survival. As global temperatures rise, Aedes aegypti females are faced with climate challenges, like intense droughts and intermittent precipitation, which create unpredictable and suboptimal conditions for the egg-laying step of their reproductive cycle. Aedes aegypti mosquitoes nonetheless show remarkable reproductive resilience, but how they achieve this is unknown. Here we show that under drought-like conditions simulated in the laboratory, mated, blood-fed Aedes aegypti females carrying mature eggs retain them in their ovaries for extended periods, while maintaining the viability of these eggs until they can be deposited in freshwater. Using transcriptomic and proteomic profiling of Aedes aegypti ovaries, we identify two previously uncharacterized genes – here named tweedledee and tweedledum – that show ovary-enriched, temporally-restricted expression during egg retention. These genes are mosquito-specific, linked within a syntenic locus, and rapidly evolving under positive selection, raising the possibility that they serve an adaptive function. Using loss-of-function mutagenesis to disrupt both genes, we show that, tweedledee and tweedledum, which encode secreted proteins, are specifically required for extended retention of viable eggs, such as during intermittent precipitation or drought. These results highlight an elegant example of taxon-restricted genes at the heart of an important adaptation that equips Aedes aegypti females with “insurance” to, when contextually appropriate, flexibly extend their reproductive sequence without losing reproductive capacity, thus allowing this species to exploit diverse and unpredictable habitats.

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Eggs of the mosquito Aedes aegypti survive desiccation by rewiring their polyamine and lipid metabolism

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