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The impact of host diet on Wolbachia titer in Drosophila.

Serbus LR, White PM, Silva JP, Rabe A, Teixeira L, Albertson R, Sullivan W - PLoS Pathog. (2015)

Bottom Line: Furthermore, genetic ablation of insulin-producing cells located in the Drosophila brain abolished the yeast impact on oocyte titer.Furthermore, dietary yeast increased somatic Wolbachia titer overall, though not in the central nervous system.These findings highlight the interactions between Wolbachia and germline cells as strongly nutrient-sensitive, and implicate conserved host signaling pathways by which nutrients influence Wolbachia titer.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Florida International University Modesto A. Maidique Campus, Miami, Florida, United States of America; Biomolecular Sciences Institute, Florida International University Modesto A. Maidique Campus, Miami, Florida, United States of America.

ABSTRACT
While a number of studies have identified host factors that influence endosymbiont titer, little is known concerning environmental influences on titer. Here we examined nutrient impact on maternally transmitted Wolbachia endosymbionts in Drosophila. We demonstrate that Drosophila reared on sucrose- and yeast-enriched diets exhibit increased and reduced Wolbachia titers in oogenesis, respectively. The yeast-induced Wolbachia depletion is mediated in large part by the somatic TOR and insulin signaling pathways. Disrupting TORC1 with the small molecule rapamycin dramatically increases oocyte Wolbachia titer, whereas hyper-activating somatic TORC1 suppresses oocyte titer. Furthermore, genetic ablation of insulin-producing cells located in the Drosophila brain abolished the yeast impact on oocyte titer. Exposure to yeast-enriched diets altered Wolbachia nucleoid morphology in oogenesis. Furthermore, dietary yeast increased somatic Wolbachia titer overall, though not in the central nervous system. These findings highlight the interactions between Wolbachia and germline cells as strongly nutrient-sensitive, and implicate conserved host signaling pathways by which nutrients influence Wolbachia titer.

No MeSH data available.


Related in: MedlinePlus

Sucrose-enriched food elevates oocyte Wolbachia titer in a chico-dependent manner.Wolbachia were quantified within single focal planes of oocytes exposed to control food or sucrose-enriched food. The average titer detected per nutrient condition is shown. A) Impact of sucrose on oocyte Wolbachia titer in wild-type D. melanogaster. B) Comparison of oocyte Wolbachia titers between control food and other foods enriched in glucose, fructose, a mixture of glucose and fructose, or sucrose. C-E) Sucrose impact on oocyte Wolbachia titer in flies that carry tissue-specific chico RNAi disruptions. Genotypes used: C) {nos-GAL4}/+; {nos-GAL4}/{UAS-chico dsRNA}. D) {da-GAL4}/{UAS-chico dsRNA}. E) {da-GAL4}/+.
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ppat.1004777.g006: Sucrose-enriched food elevates oocyte Wolbachia titer in a chico-dependent manner.Wolbachia were quantified within single focal planes of oocytes exposed to control food or sucrose-enriched food. The average titer detected per nutrient condition is shown. A) Impact of sucrose on oocyte Wolbachia titer in wild-type D. melanogaster. B) Comparison of oocyte Wolbachia titers between control food and other foods enriched in glucose, fructose, a mixture of glucose and fructose, or sucrose. C-E) Sucrose impact on oocyte Wolbachia titer in flies that carry tissue-specific chico RNAi disruptions. Genotypes used: C) {nos-GAL4}/+; {nos-GAL4}/{UAS-chico dsRNA}. D) {da-GAL4}/{UAS-chico dsRNA}. E) {da-GAL4}/+.

Mentions: To further investigate the sensitivity of oocyte Wolbachia titer to somatic insulin signaling, we also examined the effect of a sucrose-rich, high sugar diet. High sugar diets have been shown to induce insulin resistance in Drosophila [75,76]. This is may be due in part to increased expression of NLaz [75], which in mammals is known to suppress Akt function within the insulin signaling pathway (Fig. 1) [77–79]. To test the impact of sucrose-enriched diets on oocyte Wolbachia titer, 2-day old D. melanogaster were fed standard food diluted 1/3 with saturated sucrose solution, hereafter referred to as “sucrose-enriched food” (S1 Table). After 3 days of exposure to this diet, Wolbachia titer was assessed in oogenesis. Oocytes from the sucrose-enriched condition exhibited a 2.4-fold increase in Wolbachia (Fig. 6A). Unlike oocytes raised on control food, which exhibited an average of 165 +/- 22.2 Wolbachia (n = 24), D. melanogaster oocytes exposed to sucrose-enriched food exhibited 392 +/- 25.3 Wolbachia (n = 26) (p < 0.001) (Fig. 6A). These data indicate that a high sugar diet significantly elevates oocyte Wolbachia titer, possibly via an insulin-related mechanism.


The impact of host diet on Wolbachia titer in Drosophila.

Serbus LR, White PM, Silva JP, Rabe A, Teixeira L, Albertson R, Sullivan W - PLoS Pathog. (2015)

Sucrose-enriched food elevates oocyte Wolbachia titer in a chico-dependent manner.Wolbachia were quantified within single focal planes of oocytes exposed to control food or sucrose-enriched food. The average titer detected per nutrient condition is shown. A) Impact of sucrose on oocyte Wolbachia titer in wild-type D. melanogaster. B) Comparison of oocyte Wolbachia titers between control food and other foods enriched in glucose, fructose, a mixture of glucose and fructose, or sucrose. C-E) Sucrose impact on oocyte Wolbachia titer in flies that carry tissue-specific chico RNAi disruptions. Genotypes used: C) {nos-GAL4}/+; {nos-GAL4}/{UAS-chico dsRNA}. D) {da-GAL4}/{UAS-chico dsRNA}. E) {da-GAL4}/+.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4380406&req=5

ppat.1004777.g006: Sucrose-enriched food elevates oocyte Wolbachia titer in a chico-dependent manner.Wolbachia were quantified within single focal planes of oocytes exposed to control food or sucrose-enriched food. The average titer detected per nutrient condition is shown. A) Impact of sucrose on oocyte Wolbachia titer in wild-type D. melanogaster. B) Comparison of oocyte Wolbachia titers between control food and other foods enriched in glucose, fructose, a mixture of glucose and fructose, or sucrose. C-E) Sucrose impact on oocyte Wolbachia titer in flies that carry tissue-specific chico RNAi disruptions. Genotypes used: C) {nos-GAL4}/+; {nos-GAL4}/{UAS-chico dsRNA}. D) {da-GAL4}/{UAS-chico dsRNA}. E) {da-GAL4}/+.
Mentions: To further investigate the sensitivity of oocyte Wolbachia titer to somatic insulin signaling, we also examined the effect of a sucrose-rich, high sugar diet. High sugar diets have been shown to induce insulin resistance in Drosophila [75,76]. This is may be due in part to increased expression of NLaz [75], which in mammals is known to suppress Akt function within the insulin signaling pathway (Fig. 1) [77–79]. To test the impact of sucrose-enriched diets on oocyte Wolbachia titer, 2-day old D. melanogaster were fed standard food diluted 1/3 with saturated sucrose solution, hereafter referred to as “sucrose-enriched food” (S1 Table). After 3 days of exposure to this diet, Wolbachia titer was assessed in oogenesis. Oocytes from the sucrose-enriched condition exhibited a 2.4-fold increase in Wolbachia (Fig. 6A). Unlike oocytes raised on control food, which exhibited an average of 165 +/- 22.2 Wolbachia (n = 24), D. melanogaster oocytes exposed to sucrose-enriched food exhibited 392 +/- 25.3 Wolbachia (n = 26) (p < 0.001) (Fig. 6A). These data indicate that a high sugar diet significantly elevates oocyte Wolbachia titer, possibly via an insulin-related mechanism.

Bottom Line: Furthermore, genetic ablation of insulin-producing cells located in the Drosophila brain abolished the yeast impact on oocyte titer.Furthermore, dietary yeast increased somatic Wolbachia titer overall, though not in the central nervous system.These findings highlight the interactions between Wolbachia and germline cells as strongly nutrient-sensitive, and implicate conserved host signaling pathways by which nutrients influence Wolbachia titer.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Florida International University Modesto A. Maidique Campus, Miami, Florida, United States of America; Biomolecular Sciences Institute, Florida International University Modesto A. Maidique Campus, Miami, Florida, United States of America.

ABSTRACT
While a number of studies have identified host factors that influence endosymbiont titer, little is known concerning environmental influences on titer. Here we examined nutrient impact on maternally transmitted Wolbachia endosymbionts in Drosophila. We demonstrate that Drosophila reared on sucrose- and yeast-enriched diets exhibit increased and reduced Wolbachia titers in oogenesis, respectively. The yeast-induced Wolbachia depletion is mediated in large part by the somatic TOR and insulin signaling pathways. Disrupting TORC1 with the small molecule rapamycin dramatically increases oocyte Wolbachia titer, whereas hyper-activating somatic TORC1 suppresses oocyte titer. Furthermore, genetic ablation of insulin-producing cells located in the Drosophila brain abolished the yeast impact on oocyte titer. Exposure to yeast-enriched diets altered Wolbachia nucleoid morphology in oogenesis. Furthermore, dietary yeast increased somatic Wolbachia titer overall, though not in the central nervous system. These findings highlight the interactions between Wolbachia and germline cells as strongly nutrient-sensitive, and implicate conserved host signaling pathways by which nutrients influence Wolbachia titer.

No MeSH data available.


Related in: MedlinePlus