Abstract
Mortality in insects consuming high-protein-and-low-carbohydrate diets resembles a type III lifespan curve with increased mortality at an early age and few survivors that live a relatively long lifespan. We selected for a Drosophila line able to live for a long time on an imbalanced high-protein-low-carbohydrate diet by carrying out five rounds of breeding to select for the most long-lived survivors. Adaptation to this diet in the selected line was studied at the biochemical, physiological and transcriptomic levels. The selected line of flies consumed less of the imbalanced food but also accumulated more storage metabolites: glycogen, triacylglycerides, and trehalose. Selected flies also had a higher activity of alanine transaminase and a higher urea content. Adaptation of the selected line on the transcriptomic level was characterized by down-regulation of genes encoding serine endopeptidases (Jon25i, Jon25ii, betaTry, and others) but up-regulation of genes encoding proteins related to the immune system, such as antimicrobial peptides, Turandot-family humoral factors, hexamerin isoforms, and vitellogenin. These sets of down- and up-regulated genes were similar to those observed in fruit flies with suppressed juvenile hormone signaling. Our data show that the physiological adaptation of fruit flies to a high-protein-low-carbohydrate diet occurs via intuitive pathways, namely a decrease in food consumption, conversion of amino acids into ketoacids to compensate for the lack of carbohydrate, and accumulation of storage metabolites to eliminate the negative effects of excess amino acids. Nevertheless, transcriptomic adaptation occurs in a counter-intuitive way likely via an influence of gut microbiota on food digestion.
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This work is partially supported via a grant from the Ministry of Education and Science of Ukraine to OL (#0117U006426) and discovery grant from the Natural Sciences and Engineering Research Council of Canada (#6793) to KBS.
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OL, SJS, ISY: conceptualization; OL, ISY, SJS: methodology; OL, ISY, SJS, LJG: formal analysis; OL, ISY, SJS, LJG, NIB: investigation; OL and SJS: resources; OL, YIS: data curation; OL, ISY, DVG, LJG: preparation of original draft; SJS, KBS: writing, review and editing; OL, ISY: visualization; OL, ISY: supervision.
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10522_2020_9880_MOESM1_ESM.tif
Fig. S1 Effect of optimal and high P:C diets on the survival of Canton S and Oregon R fly lines. We confirmed the phenotype obtained from the W1118 line in the first round of selection on high P:C food. Lifespan of Canton S male (A) and female (B) flies was dramatically lower on the high P:C diet, as well as survival of Oregon R males (C) and females (D) but a small fraction lived almost 40-60 days. Each curve represents the percentage of individuals alive as a function of age. Differences between curves were analyzed using log-rank test. Supplementary file1 (TIF 0 kb)
10522_2020_9880_MOESM2_ESM.tif
Fig. S2 Survival of flies from control and transferred cohorts. Lifespan on optimal P:C diet (control) over all rounds of selection was not significantly affected in male (A) and female (B) flies. Offspring males (C) and females (D) from optimal P:C diet were transferred to high P:C diet after each round of selection. Shifting to high P:C diet did not extend the lifespan, confirming the requirement for a few selection rounds to evolve adaptation to a high P:C diet. Each curve represents the percentage of individuals alive as a function of age. Differences between curves were analyzed using a log-rank test. Supplementary file2 (TIF 0 kb)
10522_2020_9880_MOESM3_ESM.tif
Fig. S3 Effect of adaptation to a high P:C diet on fecundity, body weight and stress resistance. Flies selected on high P:C diet laid significantly more eggs after each round of selection vs. control flies. The flies laid eggs during 48 hours. Then the number of eggs was recalculated as an average of eggs per fly, per 24 hours. (A). Body weight of male (B) and female (C) flies was not significantly different over all rounds of selection. There was no difference in starvation resistance of males (D) after selection but survival of starved females (E) selected on the high P:C diet was higher (P<0.0001 by log-rank test). Fecundity and body weight values are expressed as mean ± S.E.M. with values considered significantly different if P<0.05. Each starvation resistance curve represents percentage of individuals alive as a function of starvation time in hours. Differences between curves were analyzed using log-rank test with P<0.0001. Supplementary file3 (TIF 0 kb)
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Yurkevych, I.S., Gray, L.J., Gospodaryov, D.V. et al. Development of fly tolerance to consuming a high-protein diet requires physiological, metabolic and transcriptional changes. Biogerontology 21, 619–636 (2020). https://doi.org/10.1007/s10522-020-09880-0
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DOI: https://doi.org/10.1007/s10522-020-09880-0