Zika virus is a mosquito-borne disease that can cause severe birth defects and neurological complications in humans.
It is transmitted by the bite of an infected Aedes aegypti mosquito, which is also responsible for spreading dengue, yellow fever, and chikungunya.
These mosquitoes are widely distributed in tropical and subtropical regions of the world, and have adapted to urban environments where they breed in small containers of water.
One of the remarkable features of Aedes aegypti mosquitoes is their ability to survive desiccation, or drying out, of their eggs.
Unlike most other insects, Aedes aegypti eggs can withstand long periods of drought and hatch when they encounter water again. This allows them to persist in harsh conditions and colonize new areas.
However, the molecular mechanisms behind this phenomenon are poorly understood.
A new study published on October 24th in the open-access journal PLOS Biology by Anjana Prasad, Sunil Laxman, and colleagues at the Institute for Stem Cell Science and Regenerative Medicine in Bengaluru, India and the Indian Institute of Technology in Mandi, India, sheds light on how eggs of the Zika-carrying mosquito survive desiccation.
The researchers used a combination of proteomics, metabolomics, and gene expression analysis to compare the changes in egg proteins, metabolites, and genes before and after desiccation.
They discovered that the eggs undergo a major metabolic shift that enables them to cope with water loss and oxidative stress.
Metabolic changes in desiccated eggs
(Photo : OLIVIER MORIN/AFP via Getty Images)
The researchers first showed that Aedes aegypti eggs must be at least 15 hours old to survive desiccation; eggs that were dried out before this stage failed to hatch when rehydrated.
They then collected eggs at different developmental stages and subjected them to desiccation for 24 hours.
They found that the survival rate of the eggs increased with age, reaching up to 90% for 72-hour-old eggs.
To understand how the eggs tolerate desiccation, the researchers analyzed the changes in their protein and metabolite profiles using mass spectrometry.
They identified over 2,000 proteins and 300 metabolites that were differentially expressed between hydrated and desiccated eggs.
They found that desiccated eggs had lower levels of proteins and metabolites involved in glycolysis and the tricarboxylic acid (TCA) cycle, which are pathways that generate energy from glucose.
Instead, they had higher levels of proteins and metabolites involved in fatty acid metabolism, which is an alternative source of energy that requires less water.
The researchers also observed that desiccated eggs had higher levels of amino acids such as arginine and glutamine, which are precursors for polyamines.
Polyamines are small molecules that can protect cellular structures from damage caused by dehydration and oxidation.
The researchers confirmed that polyamine levels increased in desiccated eggs using a fluorescent probe.
They also showed that blocking polyamine synthesis with an inhibitor reduced the survival rate of desiccated eggs.
In addition, the researchers found that desiccated eggs had higher levels of proteins and metabolites involved in antioxidant defense, such as glutathione and catalase.
These molecules can scavenge reactive oxygen species (ROS) that are generated during desiccation and cause oxidative stress.
The researchers measured ROS levels in hydrated and desiccated eggs using another fluorescent probe and found that they were significantly higher in desiccated eggs.
Moreover, they showed that blocking antioxidant enzymes with inhibitors increased ROS levels and reduced the survival rate of desiccated eggs.
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Gene expression changes in desiccated eggs
To complement their proteomic and metabolomic analyses, the researchers performed RNA sequencing to examine the changes in gene expression between hydrated and desiccated eggs.
They identified over 1,000 genes that were differentially expressed, with most of them being downregulated in desiccated eggs.
They found that many of these genes were involved in metabolic processes, such as glycolysis, TCA cycle, fatty acid metabolism, polyamine synthesis, and antioxidant defense.
This suggested that the changes in protein and metabolite levels were regulated at the transcriptional level.
The researchers also identified several transcription factors that were differentially expressed between hydrated and desiccated eggs.
These included members of the heat shock factor (HSF), nuclear factor kappa B (NF-κB), forkhead box O (FOXO), peroxisome proliferator-activated receptor (PPAR), hypoxia-inducible factor (HIF), and cAMP response element-binding protein (CREB) families.
These transcription factors are known to regulate stress responses in various organisms, including insects.
The researchers hypothesized that they may play a role in orchestrating the metabolic changes in desiccated eggs.
To test this hypothesis, the researchers used RNA interference (RNAi) to knock down the expression of some of these transcription factors in eggs and assessed their survival after desiccation.
They found that knocking down HSF1, NF-κB, FOXO, and PPARγ significantly reduced the survival rate of desiccated eggs, while knocking down HIF1α and CREB had no effect.
These results suggested that these transcription factors are essential for the desiccation tolerance of Aedes aegypti eggs.
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