Abstract
Dietary essential amino acids have an important influence on the lifespan and fitness of animals. The expression of the NAD+-dependent histone deacetylase, Sir2, can be influenced by diet, but its role in the extension of lifespan has recently been challenged. Here, we used the honeybee to test how the dietary balance of carbohydrates and essential amino acids and/or Sir2 affected lifespan. Using liquid diets varying in their ratio of essential amino acids to carbohydrate (EAA:C), we found that adult worker bees fed diets high in essential amino acids (≥1:10) had shorter lifespans than bees fed diets containing low levels of dietary amino acids. Bees fed a 1:500 EAA:C diet lived longer and, in contrast to bees fed any of the other diets, expressed Sir2 at levels tenfold higher or more than bees fed a 1:5 EAA:C diet. When bees were fed the 1:500 diet, small interfering RNA (siRNA)-mediated knock-down of Sir2 expression shortened lifespan but did not reduce survival to the same extent as the 1:5 diet, indicating that Sir2 contributes to mechanisms that determine lifespan in response to differences in macronutrient intake but is not the sole determinant. These data show that the ratio of dietary amino acids to carbohydrate influences Sir2 expression and clearly demonstrate that Sir2 is one of the factors that can determine honeybee lifespan. We propose that effects of dietary amino acids and Sir2 on lifespan may depend on the simultaneous activation of multiple nutrient sensors that respond to relative levels of essential amino acids and carbohydrates.Electronic supplementary materialThe online version of this article (doi:10.1007/s11357-014-9649-9) contains supplementary material, which is available to authorized users.
Highlights
The quantity and quality of food an animal eats directly affects its lifespan and fitness
The pilot experiment to explore the effect of a range of different dietary essential amino acids to carbohydrate (EAA):C ratios on survival revealed that bees fed a 1:5 diet had higher mortality than bees on all other diets we tested
In the follow-up independent experiment conducted over the full lifespan to compare the effects of the 1:500 and 1:5 diets, we found that honeybees fed on the high amino acid diet (1:5) were 30 times more likely to die prematurely than those fed the 1:500 diet [Fig. 1a; Cox regression (Coxreg), 1:5×1:500, χ12=84.8, hazard ratio (HR)=30 (95 % confidence interval (CI) 14–63), P
Summary
The quantity and quality of food an animal eats directly affects its lifespan and fitness. Elevated levels of certain amino acids (Grandison et al 2009) and protein (Altaye et al 2010; Lagiou et al 2007) can reduce survival It is unclear whether the effect of diet on lifespan is a function of energy intake, dietary amino acids and proteins, or both. In yeast (Saccharomyces cerevisiae), C. elegans and Drosophila, mutants that over-express Sir live longer, and mutants with reduced or no Sir gene function are not sensitive to the effects of diet on lifespan (Kaeberlein et al 1999; Tissenbaum and Guarente 2001; Rogina and Helfand 2004). We show unequivocally that Sir in honeybees is one of the determinants of lifespan when the diet provides amino acids at this ratio by demonstrating a reduction in lifespan under conditions of Sir knockdown by siRNA
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