High carbohydrate–low protein consumption maximizes Drosophila lifespan

Bruce, Kimberley D.; Hoxha, Sany; Carvalho, Gil B.; Yamada, Ryuichi; Wang, Horng-Dar; Karayan, Paul; He, Shan; Brummel, Ted; Kapahi, Pankaj; Ja, William W.

doi:10.1016/j.exger.2013.02.003

Cited by 116 publications

(138 citation statements)

References 38 publications

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“…Specifically, an addition of 10% sucrose reduces the number of eggs by less than 50% (Bass et al 2007), whereas 10% ethanol drops fecundity to near zero in both bacterial treatments. Second, increasing dietary sugar typically increases fly lifespan (Galenza et al 2016;Bruce et al 2013;Lee et al 2008), whereas our study found that ethanol has a negative effect on lifespan regardless of whether bacteria are present (although this trend is only apparent at high ethanol concentrations for the bacterially-colonized treatment). Third, we found that ethanol does not lead to the typical tradeoff between lifespan and fecundity observed by varying nutrients (Zera & Harshman 2001;Djawdan et al 1996) -instead we found that ethanol decreases both components of fitness (Figures 1 and 2).…”

Section: Ethanol As a Toxincontrasting

confidence: 49%

Chronic ethanol ingestion impairs Drosophila melanogaster health in a microbiome-dependent manner

Chandler

Innocent

Huang

et al. 2017

Preprint

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The microbiome can modulate the interaction between animals and their environment. In particular, intestinal microbes play a strong role in shaping how animals respond to their diets, and especially dietary toxins. In this study, we investigated how the microbiome affects the interaction between the fruit fly Drosophila melanogaster and ingested ethanol. D. melanogaster naturally feeds on fermenting fruits and therefore commonly ingests ethanol. This dietary ethanol is generally considered to be a toxin, but its effect on adult fly fitness has yet to be shown. We found that the reproductive output of bacterially-colonized flies remains high with low amounts of dietary ethanol, while that of bacteria-free flies decreases precipitously after ethanol ingestion. This shows that bacteria protect D. melanogaster from the damaging effects of ingested ethanol, which has important implications for fitness under natural conditions. We also observed that bacterial colonization and ethanol both negatively affect fly lifespan. In particular, bacteria play a dominant role on fly lifespan and therefore the negative effects of ethanol are only observed in bacteria-free flies. We next asked how the bacterial microbiota changes in response to dietary ethanol. Contrary to our expectations, we found that total bacterial abundance stays relatively constant with increasing ethanol. In vivo survival of bacteria was well above the in vitro toxic dose of ethanol, demonstrating that the host is shielding the microbiome from the negative effects of ethanol. Next, we investigated several aspects of host physiology that may underlie bacterially-modulated fitness changes. We found that regardless of bacterial colonization, ethanol ingestion decreases the prevalence of intestinal barrier failure and increases fly body fat content, suggesting these mechanisms are not directly responsible for bacteria-dependent fitness differences. Finally, measurements of dietary ethanol content suggest that bacterial metabolism can only partially explain the observed fitness effects. Overall, we found significant bacteria-byethanol interactions on D. melanogaster and that bacteria ameliorate the negative effects of ethanol on host fecundity. Because of the central role of ethanol in the ecology of D. melanogaster, these results have important implications for our understanding of fruit fly natural history. More generally, they underscore the importance of the microbiome in shaping an animal's interaction with its environment.

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Section: Ethanol As a Toxincontrasting

confidence: 49%

Chronic ethanol ingestion impairs Drosophila melanogaster health in a microbiome-dependent manner

Chandler

Innocent

Huang

et al. 2017

Preprint

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“…n = 658 flies, C; 482, D; 598, C to D switch; 500, C + H 2 O; 621, C to C + H 2 O switch. (D) In a paradigm varying carbohydrate:protein ratio, which affects lifespan in a nutrient-dependent manner (43,44), an acute switch from HP to LP diet results in an intermediate trajectory consistent with the deceleration model and similar in nature to-albeit milder than-the effect of temperature (B). All postswitch trajectories are significantly different (Table S1).…”

Section: Discussionmentioning

confidence: 99%

“…Fly food was prepared as described previously (43,44). The concentrated (C) diet contained 10% yeast extract and 10% sucrose, while the diluted (D) diet contained 2.5% yeast extract and 2.5% sucrose, both in 1% agar (all wt/vol).…”

Section: Methodsmentioning

confidence: 99%

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The 4E-BP growth pathway regulates the effect of ambient temperature on Drosophila metabolism and lifespan

Carvalho

Drago

Hoxha

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Changes in body temperature can profoundly affect survival. The dramatic longevity-enhancing effect of cold has long been known in organisms ranging from invertebrates to mammals, yet the underlying mechanisms have only recently begun to be uncovered. In the nematode Caenorhabditis elegans, this process is regulated by a thermosensitive membrane TRP channel and the DAF-16/FOXO transcription factor, but in more complex organisms the underpinnings of cold-induced longevity remain largely mysterious. We report that, in Drosophila melanogaster, variation in ambient temperature triggers metabolic changes in protein translation, mitochondrial protein synthesis, and posttranslational regulation of the translation repressor, 4E-BP (eukaryotic translation initiation factor 4E-binding protein). We show that 4E-BP determines Drosophila lifespan in the context of temperature changes, revealing a genetic mechanism for cold-induced longevity in this model organism. Our results suggest that the 4E-BP pathway, chiefly thought of as a nutrient sensor, may represent a master metabolic switch responding to diverse environmental factors.S tudies on the biological underpinnings of aging have uncovered numerous genetic and environmental factors regulating animal lifespan. Longevity-promoting genes include components of the insulin-like signaling pathway, the histone deacetylase Sir2, the GTPase Ras, TRP membrane channels, and transcription factors, among many others (1, 2). Environmental manipulations extending life include changes in nutrition (often referred to as caloric or dietary restriction), sexual/reproductive history, and ambient temperature (3-5).Of the factors known to impact aging, temperature is arguably the most promising. Lifespan extension by cold is evolutionarily conserved-documented in poikilotherms, such as worms and flies, and homeotherms, including mammals (4, 6-11)-and more robust than well-studied interventions such as dietary restriction (12, 13). However, the underlying mechanisms remain incompletely understood (10,14,15). In Caenorhabditis elegans, the effect of cold on survival involves the thermosensitive membrane channel TRPA-1 acting upstream of the DAF-16/FOXO transcription factor (14,15). This seminal finding countered the notion that longevity is the passive result of general thermodynamic changes, and favored instead the view that genetic pathways actively control lifespan in response to ambient temperature. However, these results have to date not been extended or replicated in other model organisms. Explanatory theories for the effect of cold on longevity include a reduction in reactive oxygen species generated by mitochondrial uncoupling proteins, suppression of autoimmune response, and changes in neuroendocrine factors (6,16,17), but these views remain largely speculative given the lack of further mechanistic insight into lifespan extension by cold in model organisms.We report that, in Drosophila, changes in temperature trigger a metabolic program impacting protein translation, mitochondrial prot...

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“…Indeed, it is now accepted that, the caloric content being constant, the proteins/carbohydrates ratio modulates lifespan, for instance in Drosophila melanogaster flies (e.g. Vigne and Frelin, 2007ab, Lee et al, 2008, Bruce et al, 2013, Zajitschek et al, 2013 and in mice (Solon-Biet et al, 2014). Therefore, the mainstream hypothesis to explain the positive effect of dietary restriction (DR) on lifespan, when observed, is now more subtle than it was, because it deals with the ratio of nutrients rather than simply with the number of calories.…”

Section: Introductionmentioning

confidence: 99%

Feeding on frozen live yeast has some deleterious effects in Drosophila melanogaster

Bourg

Gauthier

Colinet

2015

Experimental Gerontology

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Colinet. Feeding on frozen live yeast has some deleterious effects in Drosophila melanogaster. Experimental Gerontology, Elsevier, 2015, 69, pp.202-210. 10 severe stresses and behaviour in Drosophila melanogaster flies. The present study tested whether feeding flies with frozen yeast rather than with fresh yeast could have some effect on these traits, the other components of the food being similar in the two groups. Freezing altered live yeast quality and flies feeding on frozen yeast lived slightly less (males), were less fecund at older ages, and poorly resisted to some severe stresses (cold and starvation), no negative effect being observed on resistance to heat. It seems that, like in humans, feeding on a low quality food can negatively impact healthspan and that an appropriate food is not only a food with optimal number of calories and appropriate ratios of proteins, carbohydrates, and fat.

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High carbohydrate–low protein consumption maximizes Drosophila lifespan

Cited by 116 publications

References 38 publications

Chronic ethanol ingestion impairs Drosophila melanogaster health in a microbiome-dependent manner

Chronic ethanol ingestion impairs Drosophila melanogaster health in a microbiome-dependent manner

The 4E-BP growth pathway regulates the effect of ambient temperature on Drosophila metabolism and lifespan

Feeding on frozen live yeast has some deleterious effects in Drosophila melanogaster

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