Dietary and microbiome factors determine longevity in Caenorhabditis elegans

Abstract

Diet composition affects organismal health. Nutrient uptake depends on the microbiome. Caenorhabditis elegans fed a Bacillus subtilis diet live longer than those fed the standard Escherichia coli diet. Here we report that this longevity difference is primarily caused by dietary coQ, an antioxidant synthesized by E. coli but not by B. subtilis. CoQ-supplemented E. coli fed worms have a lower oxidation state yet live shorter than coQ-less B. subtilis fed worms. We showed that mutations affecting longevity for E. coli fed worms do not always lead to similar effects when worms are fed B. subtilis. We propose that coQ supplementation by the E. coli diet alters the worm cellular REDOX homeostasis, thus decreasing longevity. Our results highlight the importance of microbiome factors in longevity, argue that antioxidant supplementation can be detrimental, and suggest that the C. elegans standard E. coli diet can alter the effect of signaling pathways on longevity.

Mechanical properties measured by atomic force microscopy define health biomarkers in ageing C. elegans

“…5a, Supplementary Data 2), whereas worms fed on C. aquatica were short-lived when compared with worms fed on E. coli OP50 (−7.47%, log rank p < 0.001, Fig. 5a, Supplementary Data 2), as previously reported [54][55][56] . Interestingly, longitudinal stiffness measurements showed that E. coli diets, though being standard laboratory food, are surprisingly detrimental to the maintenance of stiffness with age when compared with worms on either B. subtilis (B. subtilis vs OP50 at day 12 FC = 5.79, t test p < 0.0001; B. subtilis vs OP50 at mean lifespan FC = 4.10, t test p < 0.0001) or C. aquatica diets (C. aquatica vs OP50 at day 12 FC = 4.14, t test p < 0.0001; C. aquatica vs OP50 at mean lifespan FC = 4.32, t test p < 0.0001; Fig.…”

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“…B. subtilis are Gram-positive bacteria, consequently they lack the outer lipid membrane [42]. Despite cell structure differences, B. subtilis and E. coli have been reported to have a similar caloric content as the main calorie contribution is conferred by proteins and carbohydrates and not by the lipid fraction [11]. It is however plausible that the different lipid composition and distribution found in these two types of bacteria, 80% of phosphatidylethanolamine in the membrane lipids of E. coli versus 12% in B. subtilis [40], causes up-regulation of specific sets of genes required for E. coli digestion and metabolism of its components such as carboxylic acids.…”

“…subtilis fed worms live substantially longer than worms grown on E. coli [6] and these diets appear to induce different causes of death to the worms [8,49]. It has been recently proposed that the C. elegans life span difference observed when the worm diet is changed from the standard E. coli to B. subtilis is mainly due to the persistent antioxidant effect of CoQ present in the E. coli diet, which leads to an imbalance in cellular REDOX homeostasis [11]. Feeding worms E. coli or B. subtilis diets can considerably affect the life span of the worms, consequently E. coli fed worms will display an older physiological age than B. subtilis fed worms with the same chronological age.…”

“…Bacillus subtilis, a common soil bacterium, has been used as an alternative C. elegans diet in a number of C. elegans studies [6][7][8][9][10][11]. B. subtilis has a similar caloric and nutrition content as E. coli [11].…”

“…B. subtilis has a similar caloric and nutrition content as E. coli [11]. High-energy demanding metabolic processes such as egg production and developmental growth are comparable when worms are fed E. coli or B. subtilis [11]. Interestingly, the mean life span of E. coli fed worms maintained at 20ºC has been shown to be around 17 days, compared to 27 days for B. subtilis fed worms maintained at the same temperature [6,8].…”