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

View Article: PubMed Central - PubMed

ABSTRACT

Background: Exercise 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.

Results: Here, 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.

Conclusions: In 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 material: The online version of this article (doi:10.1186/s12915-017-0368-4) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus

C. elegans get tired after acute swim exercise. a The acute swim exercise (M9 buffer) and control (unseeded plate crawl) protocol for C. elegans. b Crawling distance traveled by N2 animals at different time points after a 90 min swim exercise. Each point represents a single animal (n = 49–50 animals). c Crawling distance ratio of exercise to control N2 animals 5 min after a swim exercise of displayed durations (n = 40–50 animals). Unpaired two-tailed Student’s t test was used in (b) and (c) to compare crawling distances of control versus exercise animals. *P < 0.05; ****P < 0.0001. NGM nematode growth medium, ns non-significant
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Fig2: C. elegans get tired after acute swim exercise. a The acute swim exercise (M9 buffer) and control (unseeded plate crawl) protocol for C. elegans. b Crawling distance traveled by N2 animals at different time points after a 90 min swim exercise. Each point represents a single animal (n = 49–50 animals). c Crawling distance ratio of exercise to control N2 animals 5 min after a swim exercise of displayed durations (n = 40–50 animals). Unpaired two-tailed Student’s t test was used in (b) and (c) to compare crawling distances of control versus exercise animals. *P < 0.05; ****P < 0.0001. NGM nematode growth medium, ns non-significant

Mentions: Young adult C. elegans swim continuously in M9 buffer for just over 90 min before entering an episodic phase during which periods of active swimming alternate with periods of quiescence [19]. For that reason, we decided to adopt an acute exercise protocol in which young adult C. elegans continuously swam in M9 buffer up to the 90 min transition point and were then returned to a bacterially seeded nematode growth medium (NGM) agar plate. We transferred crawling control animals for the same 90 min to an unseeded NGM agar plate (Fig. 2a). This experimental design guaranteed that any differences observed between exercised and control animals were not due to differences in food availability or to the rough handling associated with pick-mediated transfer of animals. For all the experiments presented here, samples were collected either immediately before exercise or at different time points post-exercise.Fig. 2


Single swim sessions in C. elegans induce key features of mammalian exercise
C. elegans get tired after acute swim exercise. a The acute swim exercise (M9 buffer) and control (unseeded plate crawl) protocol for C. elegans. b Crawling distance traveled by N2 animals at different time points after a 90 min swim exercise. Each point represents a single animal (n = 49–50 animals). c Crawling distance ratio of exercise to control N2 animals 5 min after a swim exercise of displayed durations (n = 40–50 animals). Unpaired two-tailed Student’s t test was used in (b) and (c) to compare crawling distances of control versus exercise animals. *P < 0.05; ****P < 0.0001. NGM nematode growth medium, ns non-significant
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5385602&req=5

Fig2: C. elegans get tired after acute swim exercise. a The acute swim exercise (M9 buffer) and control (unseeded plate crawl) protocol for C. elegans. b Crawling distance traveled by N2 animals at different time points after a 90 min swim exercise. Each point represents a single animal (n = 49–50 animals). c Crawling distance ratio of exercise to control N2 animals 5 min after a swim exercise of displayed durations (n = 40–50 animals). Unpaired two-tailed Student’s t test was used in (b) and (c) to compare crawling distances of control versus exercise animals. *P < 0.05; ****P < 0.0001. NGM nematode growth medium, ns non-significant
Mentions: Young adult C. elegans swim continuously in M9 buffer for just over 90 min before entering an episodic phase during which periods of active swimming alternate with periods of quiescence [19]. For that reason, we decided to adopt an acute exercise protocol in which young adult C. elegans continuously swam in M9 buffer up to the 90 min transition point and were then returned to a bacterially seeded nematode growth medium (NGM) agar plate. We transferred crawling control animals for the same 90 min to an unseeded NGM agar plate (Fig. 2a). This experimental design guaranteed that any differences observed between exercised and control animals were not due to differences in food availability or to the rough handling associated with pick-mediated transfer of animals. For all the experiments presented here, samples were collected either immediately before exercise or at different time points post-exercise.Fig. 2

View Article: PubMed Central - PubMed

ABSTRACT

Background: Exercise 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.

Results: Here, 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&nbsp;min specifically consumed muscle fat supplies and exhibited post-swim locomotory fatigue, with both muscle fat depletion and fatigue indicators recovering within 1&nbsp;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&nbsp;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&nbsp;hours post-exercise.

Conclusions: In 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 material: The online version of this article (doi:10.1186/s12915-017-0368-4) contains supplementary material, which is available to authorized users.

No MeSH data available.


Related in: MedlinePlus