How eggs of the Zika-carrying mosquito survive desiccation
Identification of metabolic pathway points to new control opportunities
Peer-Reviewed PublicationIMAGE:
A MALE AND A FEMALE AEDES MOSQUITO, TAKEN IN THE RESEARCHERS’ LAB.
view moreCREDIT: ANJANA PRASAD (CC-BY 4.0, HTTPS://CREATIVECOMMONS.ORG/LICENSES/BY/4.0/)
Eggs of the mosquito that carries Zika virus can tolerate extended desiccation by altering their metabolism, according to a new study publishing 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. The finding offers potential new ways to control the spread of this mosquito.
Cells are made mostly of water, and desiccation is a potentially fatal event for any organism, since the structures of many proteins and other cellular molecules are dependent on adequate hydration. While many types of microbes have evolved mechanisms to survive drying out, only a few animals have. Among them is the mosquito Aedes aegypti, the carrier of a variety of viral diseases, including, Zika, dengue, yellow fever, and Chikungunya. Originally found in North Africa, Ae. aegypti has expanded globally, and is now a threat in warm, moist regions throughout the world.
Aedes eggs require from 48 to 72 hours to hatch into larvae, and the authors first showed that 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 compared the proteomes of viable eggs that had and had not been desiccated, and found multiple major changes in metabolic pathways within the desiccated eggs. These included increases in the levels of those enzymes in the tricarboxylic acid (Krebs) cycle that promote lipid metabolism, and a decrease in enzymes of glycolysis and ATP-producing parts of the TCA cycle, which together shunted cellular metabolism toward the production and use of fatty acids. Overall, the level of metabolism was reduced, while the levels of the amino acids arginine and glutamine were increased. In addition, enzymes that reduce the damaging effects of oxidative stress, a known consequence of dehydration, were also increased.
When linked together, arginine molecules form polyamines, which are known to help protect nucleic acids, proteins, and membranes from a variety of insults. Here, the authors showed that the eggs accumulate polyamines, suggesting that they may be a key aspect of desiccation tolerance. To test this, they fed egg-laying female mosquitoes an inhibitor of polyamine synthesis. The eggs that they laid were significantly less able to survive desiccation than eggs from untreated females. A second inhibitor, this one of fatty acid metabolism, also reduced egg viability after desiccation. Finally, they showed that this fatty acid inhibitor reduced polyamine synthesis, indicating that one role of the increase in fatty acid breakdown is to supply the energy needed for production of protective polyamines.
“Given the importance of Ae. aegypti as a primary vector for numerous viral diseases that affect nearly half the world’s population,” Laxman said, “as well as the rapid geographical expansion of this mosquito vector, these results provide a foundation for reducing Aedes egg survival and global spread. Additionally, some of the specific inhibitors described here that reduce desiccation resistance in Ae. aegypti eggs, as well as new ones affecting other steps in the egg desiccation tolerance pathway, may prove useful as vector-control agents.”
Laxman adds, “Aedes mosquito eggs can indefinitely survive after drying up completely, and hatch into viable larvae. The embryos rewire their metabolism upon drying, to protect themselves through desiccation, and revive after water becomes available again.”
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In your coverage, please use this URL to provide access to the freely available paper in PLOS Biology: http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3002342
Citation: Prasad A, Sreedharan S, Bakthavachalu B, Laxman S (2023) Eggs of the mosquito Aedes aegypti survive desiccation by rewiring their polyamine and lipid metabolism. PLoS Biol 21(10): e3002342. https://doi.org/10.1371/journal.pbio.3002342
Author Countries: India
Funding: No specific funding was obtained for this study. DST-INSPIRE (IF190149 to SS) and DBT/Wellcome Trust India Alliance (IA/I/19/1/504286 to BB) supported individual fellowships. These funders had no role in study design, data collection and analysis, support for experiments, decision to publish, or preparation of the manuscript. Intramural support was provided by the Tata Institute for Genetics and Society (to BB), and DBT-inStem (to SL).
JOURNAL
PLoS Biology
METHOD OF RESEARCH
Experimental study
SUBJECT OF RESEARCH
Animals
How mosquito-controlling bacteria might also enhance insect fertility
Biological mechanisms found in fruit flies could inform efforts against disease-spreading mosquitos
IMAGE:
A MEI-P26 MUTANT DROSOPHILA MELANOGASTER OVARIOLE INFECTED WITH WMEL BACTERIAL SYMBIONTS. DNA IS STAINED IN RED, ANTI-VASA PROTEIN IS STAINED BLUE, AND ANTI-HU-LI TAI SHAO RING CANAL PROTEIN IS STAINED CYAN.
view moreCREDIT: SHELBI RUSSELL (CC-BY 4.0, HTTPS://CREATIVECOMMONS.ORG/LICENSES/BY/4.0/)
A new study reveals biological mechanisms by which a specific strain of bacteria in the Wolbachia genus might enhance the fertility of the insects it infects—with potentially important implications for mosquito-control strategies. Shelbi Russell of the University of California Santa Cruz, US, and colleagues report these findings in the open access journal PLOS Biology on October 24th.
Different strains of Wolbachia bacteria naturally infect a number of different animals worldwide, such as mosquitos, butterflies, and fruit flies. Wolbachia can manipulate the fertility of their hosts through a specific biological mechanism that aids the spread of Wolbachia within host populations. In recent years, people have harnessed that mechanism in strategies to deliberately infect mosquitos with a specific Wolbachia strain, reducing targeted mosquito populations and thereby potentially reducing the spread of human viruses carried by mosquitos, such as dengue or Zika.
Research in fruit flies suggests that that same strain, which is native to fruit flies, may also enhance insect fertility, with potentially important implications for mosquito control. Evidence suggests that biological processes involving the fruit-fly protein meiotic-P26 (“mei-P26"), which is essential for fruit-fly reproduction, may underlie this enhanced fertility. However, these processes have remained unclear.
To investigate, Russell and colleagues bred fruit flies with various defects affecting mei-P26—resulting in reduced fruit-fly fertility—and examined what happened when they then infected the flies with the fruit-fly-native Wolbachia strain.
They found that Wolbachia infection restored fertility in fruit flies with various mei-P26 defects, enabling them to produce more offspring than uninfected flies. Further experiments revealed how Wolbachia may restore fertility by mitigating certain perturbing effects of mei-P26 defects on specific genes and proteins, thereby resolving problems with the stem cells that produce fruit fly eggs and sperm.
In additional experiments, Wolbachia infection also enhanced the fertility of fruit flies without mei-P26 defects, resulting in higher egg lay and hatch rates.
These findings help to resolve the mystery of how this particular Wolbachia strain enhances fruit-fly fertility. Further research will be needed to better understand these effects and their potential implications for strategies that employ this strain to control mosquito populations.
Russell adds, “Wolbachia endosymbionts exist at high infection frequencies in many host populations, despite exhibiting weak gene drive systems and unobserved impacts on host fitness. Here, we show that the wMel strain of Wolbachia is able to rescue and reinforce host fertility, demonstrating their capacity to function as a beneficial symbiont.”
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In your coverage, please use this URL to provide access to the freely available paper in PLOS Biology: http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3002335
Citation: Russell SL, Castillo JR, Sullivan WT (2023) Wolbachia endosymbionts manipulate the self-renewal and differentiation of germline stem cells to reinforce fertility of their fruit fly host. PLoS Biol 21(10): e3002335. https://doi.org/10.1371/journal.pbio.3002335
Author Countries: United States
Funding: This work was supported by the UC Santa Cruz Chancellor’s Postdoctoral Fellowship and the NIH (R00GM135583 to SLR; R35GM139595 to WTS). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
JOURNAL
PLoS Biology
METHOD OF RESEARCH
Experimental study
SUBJECT OF RESEARCH
Animals
COI STATEMENT
Competing interests: The authors have declared that no competing interests exist.
Bacteria can enhance host insect’s fertility with implications for disease control
IMAGE:
A MEI-P26 MUTANT DROSOPHILA MELANOGASTER OVARIOLE INFECTED WITH WMEL BACTERIAL SYMBIONTS. DNA IS STAINED IN RED, ANTI-VASA PROTEIN IS STAINED BLUE, AND ANTI-HU-LI TAI SHAO RING CANAL PROTEIN IS STAINED CYAN.
view moreCREDIT: SHELBI RUSSELL, UC SANTA CRUZ.
Mosquitoes and other insects can carry human diseases such as dengue and Zika virus, but when those insects are infected with certain strains of the bacteria Wolbachia, this bacteria reduces levels of disease in their hosts. Humans currently take advantage of this to control harmful virus populations across the world.
New research led at UC Santa Cruz reveals how the bacteria strain Wolbachia pipientis also enhances the fertility of the insects it infects, an insight that could help scientists increase the populations of mosquitoes that do not carry human disease.
“With insect population replacement approaches, they keep all the mosquitos and just add Wolbachia so that fewer viruses are carried in those mosquitoes and transmitted to humans when they bite them — and it's working really, really well,” said Shelbi Russell, an assistant professor of biomolecular engineering at UCSC who led this research. “If there is some fertility benefit of Wolbachia that could evolve over time, then we could use that to select for higher rates of mosquitos that suppress our viral transmission.”
These results were detailed in a new paper led by Russell, published today in the journal PLOS Biology. UCSC Professor of Molecular, Cell, and Developmental Biology William Sullivan is the paper’s senior author.
Humans and Wolbachia
Different strains of Wolbachia bacteria naturally infect a number of different animals worldwide, such as mosquitos, butterflies, and fruit flies. Once they infect an insect, the bacteria are able to manipulate the reproduction and development of their host to increase their own population. Humans take advantage of this to control the population size of insects that carry diseases that threaten us.
Wolbachia have developed a mechanism to poison the sperm of infected males so that if the male mates with an uninfected female, most of the potential offspring die at the very first cell division, and the rest are lost soon after. Humans have taken advantage of this to kill off insect populations.
However, research shows that later down the line once they have killed off as many uninfected hosts as possible, Wolbachia switch their evolutionary strategy to increase population levels of infected hosts. Understanding how this happens is important for avoiding unexpected consequences of human efforts to control insect populations.
“We need to understand all of these factors and their evolutionary potential if we're going to be releasing bacteria into new ecosystems,” Russell said. “They're evolving in real time, so we need to understand where these trajectories are going.”
Beyond disease prevention, controlling insect populations and range via bacteria could be an effective mechanism for crop security in the face of the changing climate.
Understanding increased fertility
The new results show that Wolbachia pipientis, which is native to fruit flies, has evolved to increase the fertility, and therefore the population size, of its fruit fly host. Previous research has found that the Wolbachia pipientis achieves this by manipulating a protein in fruit flies called Meiotic-P26 that affects fertility, but how exactly this happens was unclear.
To investigate, Russell and her colleagues bred fruit flies with various defects affecting Mei-P26, which caused them to have reduced fertility. These defects occasionally occur naturally in the wild, but are hard to track in that setting. The researchers then examined what happened when they infected the flies with Wolbachia pipientis.
They found that Wolbachia infection restored the fruit fly’s fertility, enabling them to produce even more offspring than uninfected flies. The researchers found that Wolbachia can essentially undo gene defects in their host that would otherwise cause the population to go extinct. The Wolbachia rescue their host population through several strategies, including restoring fruit fly stem cells and ensuring that egg cells properly develop.
In further experiments, the researchers also found that, beyond rescuing fruit flies with defects, the Wolbachia pipientis infection also enhances the health and fertility of fruit flies without defects, resulting in higher egg lay and hatch rates for those insects.
Wolbachia in the lab
Russell focuses on Wolbachia because it and its fruit fly hosts are relatively easy to keep alive and reproduce in the lab. Oftentimes when scientists study bacteria, their efforts are hindered because either the host, the bacteria, or both are difficult to keep alive in the lab setting — even research into common bacteria important to humans such as Chlamydia are slowed by this problem. Wolbachia and their fruit fly hosts offer a rare opportunity to understand how bacteria can change the DNA and biological processes of their host.
“Through studying this system, I can learn a lot about how these weird bacteria work and how they integrate with host biology,” Russell said. “Bacteria are able to hop into these eukaryotes and leverage some of those mechanisms that their ancestors didn't even contain the genes for. It's a really fascinating thing in general, and it's cool that we can leverage this for biological control applications.”
Russell and her lab will continue to hone in on the specific changes that occur in the genomes and gene expression of host species, and look at the fertility benefits that Wolbachia may bring to their hosts in other insect populations.
Russell led this research primarily during her time as a postdoctoral scholar in Sullivan’s lab, where she was supported by the UC Santa Cruz Chancellor’s Postdoctoral Fellowship and funding from the National Institutes of Health.
JOURNAL
PLoS Biology
METHOD OF RESEARCH
Experimental study
SUBJECT OF RESEARCH
Animals
ARTICLE TITLE
Wolbachia endosymbionts manipulate the self-renewal and differentiation of germline stem cells to reinforce fertility of their fruit fly host
ARTICLE PUBLICATION DATE
24-Oct-2023
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