Single swim sessions in C. elegans induce key features of mammalian exercise

Abstract

BackgroundExercise exerts remarkably powerful effects on metabolism and health, with anti-disease and anti-aging outcomes. Pharmacological manipulation of exercise benefit circuits might improve the health of the sedentary and the aging populations. Still, how exercised muscle signals to induce system-wide health improvement remains poorly understood. With a long-term interest in interventions that promote animal-wide health improvement, we sought to define exercise options for Caenorhabditis elegans.ResultsHere, we report on the impact of single swim sessions on C. elegans physiology. We used microcalorimetry to show that C. elegans swimming has a greater energy cost than crawling. Animals that swam continuously for 90 min specifically consumed muscle fat supplies and exhibited post-swim locomotory fatigue, with both muscle fat depletion and fatigue indicators recovering within 1 hour of exercise cessation. Quantitative polymerase chain reaction (qPCR) transcript analyses also suggested an increase in fat metabolism during the swim, followed by the downregulation of specific carbohydrate metabolism transcripts in the hours post-exercise. During a 90 min swim, muscle mitochondria matrix environments became more oxidized, as visualized by a localized mitochondrial reduction-oxidation-sensitive green fluorescent protein reporter. qPCR data supported specific transcriptional changes in oxidative stress defense genes during and immediately after a swim. Consistent with potential antioxidant defense induction, we found that a single swim session sufficed to confer protection against juglone-induced oxidative stress inflicted 4 hours post-exercise.ConclusionsIn addition to showing that even a single swim exercise bout confers physiological changes that increase robustness, our data reveal that acute swimming-induced changes share common features with some acute exercise responses reported in humans. Overall, our data validate an easily implemented swim experience as C. elegans exercise, setting the foundation for exploiting the experimental advantages of this model to genetically or pharmacologically identify the exercise-associated molecules and signaling pathways that confer system-wide health benefits.Electronic supplementary materialThe online version of this article (doi:10.1186/s12915-017-0368-4) contains supplementary material, which is available to authorized users.

Swim exercise in C. elegans extends neuromuscular and intestinal healthspan, enhances learning ability, and protects against neurodegeneration

“…Our previous analysis of single swim sessions supported that swimming is an endurance-like exercise for C. elegans [15]. In mammals, long-term endurance exercise leads to profound transcriptional changes at the muscle level, with upregulation of muscle structural genes as one of the reproducible changes [23][24][25].…”

“…We have shown previously that swimming in a liquid environment is more energetically demanding for C. elegans than the crawling motion on agar plates used in standard lab growth protocols [15]. Moreover, we showed that a single 90 min C. elegans swim session induces key features of mammalian exercise, namely locomotory fatigue, muscle mitochondrial oxidation, a transcriptional oxidative stress response, and changes in carbohydrate and fat metabolism [15].…”

Pluronic gel-based burrowing assay for rapid assessment of neuromuscular health inC. elegans

“…The animals were washed from their culture plates with chemotaxis buffer (5 mM potassium phosphate, 1 mM calcium chloride, 1 mM magnesium sulfate) until they were free of bacteria. The total time that the worms spent swimming in liquid was kept under 30 minutes to minimize fatigue [57]. Then, 5 μL of the solution containing animals was added onto the center.…”

“…RNA extraction and quantitative PCR were carried out as previously described [57]. Briefly, we collected N2 C. elegans after burrowing (~30 animals per sample) into TRIzol Reagent (Ambion) and immediately froze animals in liquid nitrogen.…”

Redox signaling modulates Rho activity and tissue contractility in theC. elegansspermatheca

“…Superoxide dismutases are responsible for converting superoxide radicals to H2O2. We tested both cytosolic superoxide dismutases, SOD-1 and SOD-5, for effects on spermathecal transit times (Blaise et al, 2009;Braeckman et al, 2016;Doonan et al, 2008;Laranjeiro et al, 2017). DIC timelapse microscopy of ovulations revealed that mutation of sod-1, but not sod-5, resulted in shorter dwell times and no change in exit time compared to wild type (Figure 4 A,B).…”