Swimming Exercise and Transient Food Deprivation in Caenorhabditis elegans Promote Mitochondrial Maintenance and Protect Against Chemical-Induced Mitotoxicity

Jessica H. Hartman,David R. Sherwood,Latasha L. Smith,Ricardo Laranjeiro,Kacy L. Gordon,Monica Driscoll,Joel N. Meyer

doi:10.1038/s41598-018-26552-9

Jessica H. Hartman, David R. Sherwood + Show 5 more

Open Access

https://doi.org/10.1038/s41598-018-26552-9

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Abstract

Exercise and caloric restriction improve health, including reducing risk of cardiovascular disease, neurological disease, and cancer. However, molecular mechanisms underlying these protections are poorly understood, partly due to the cost and time investment of mammalian long-term diet and exercise intervention studies. We subjected Caenorhabditis elegans nematodes to a 6-day, twice daily swimming exercise regimen, during which time the animals also experienced brief, transient food deprivation. Accordingly, we included a non-exercise group with the same transient food deprivation, a non-exercise control with ad libitum access to food, and a group that exercised in food-containing medium. Following these regimens, we assessed mitochondrial health and sensitivity to mitochondrial toxicants. Exercise protected against age-related decline in mitochondrial morphology in body-wall muscle. Food deprivation increased organismal basal respiration; however, exercise was the sole intervention that increased spare respiratory capacity and proton leak. We observed increased lifespan in exercised animals compared to both control and transiently food-deprived nematodes. Finally, exercised animals (and to a lesser extent, transiently food-deprived animals) were markedly protected against lethality from acute exposures to the mitotoxicants rotenone and arsenic. Thus, swimming exercise and brief food deprivation provide effective intervention in C. elegans, protecting from age-associated mitochondrial decline and providing resistance to mitotoxicant exposures.

Highlights

One reason that the mechanisms of exercise protection have not been fully characterized is the cost and time investment of long-term exercise intervention required for rodent models or human studies
Animals were washed off food plates in K-medium and either plated onto unseeded food-free plates inundated with liquid to induce swimming exercise (“exercise” group), onto unseeded food-free plates (“transient food deprivation” or “tFD” group, which features physical manipulations and food availability matched to exercise), or back onto food plates (“control” group, mechanical manipulations implemented, always have ad libitum access to food) (Fig. 1a)
We show that long-term exercise and transient food deprivation in C. elegans are protective against aging-induced changes in mitochondrial morphology in muscle and mitochondrial function in whole animals

Summary

Introduction

One reason that the mechanisms of exercise protection have not been fully characterized is the cost and time investment of long-term exercise intervention required for rodent models or human studies. We tested the benefits of exercise to C. elegans mitochondria by administering six days of twice-daily swim sessions followed by assessment of mitochondrial health one and five days following cessation of exercise. We included a non-exercise group that was subjected to an identical bout of transient food deprivation (tFD) and a control with ad libitum access to food, which allows comparison to normally cultured nematodes. Our overall objective was to assess the mitochondrial consequences of exercise and tFD in C. elegans in order to establish C. elegans as a new model for studying molecular mechanisms underlying exercise-induced benefits to organismal health

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