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Exercise Is More Effective at Altering Gut Microbial Composition and Producing Stable Changes in Lean Mass in Juvenile versus Adult Male F344 Rats

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  • Agnieszka Mika
  • Will Van Treuren
  • Antonio González
  • Jonathan J Herrera
  • Rob Knight
  • Monika Fleshner

Abstract

The mammalian intestine harbors a complex microbial ecosystem that influences many aspects of host physiology. Exposure to specific microbes early in development affects host metabolism, immune function, and behavior across the lifespan. Just as the physiology of the developing organism undergoes a period of plasticity, the developing microbial ecosystem is characterized by instability and may also be more sensitive to change. Early life thus presents a window of opportunity for manipulations that produce adaptive changes in microbial composition. Recent insights have revealed that increasing physical activity can increase the abundance of beneficial microbial species. We therefore investigated whether six weeks of wheel running initiated in the juvenile period (postnatal day 24) would produce more robust and stable changes in microbial communities versus exercise initiated in adulthood (postnatal day 70) in male F344 rats. 16S rRNA gene sequencing was used to characterize the microbial composition of juvenile versus adult runners and their sedentary counterparts across multiple time points during exercise and following exercise cessation. Alpha diversity measures revealed that the microbial communities of young runners were less even and diverse, a community structure that reflects volatility and malleability. Juvenile onset exercise altered several phyla and, notably, increased Bacteroidetes and decreased Firmicutes, a configuration associated with leanness. At the genus level of taxonomy, exercise altered more genera in juveniles than in the adults and produced patterns associated with adaptive metabolic consequences. Given the potential of these changes to contribute to a lean phenotype, we examined body composition in juvenile versus adult runners. Interestingly, exercise produced persistent increases in lean body mass in juvenile but not adult runners. Taken together, these results indicate that the impact of exercise on gut microbiota composition as well as body composition may depend on the developmental stage during which exercise is initiated.

Suggested Citation

  • Agnieszka Mika & Will Van Treuren & Antonio González & Jonathan J Herrera & Rob Knight & Monika Fleshner, 2015. "Exercise Is More Effective at Altering Gut Microbial Composition and Producing Stable Changes in Lean Mass in Juvenile versus Adult Male F344 Rats," PLOS ONE, Public Library of Science, vol. 10(5), pages 1-20, May.
  • Handle: RePEc:plo:pone00:0125889
    DOI: 10.1371/journal.pone.0125889
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    References listed on IDEAS

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    1. Peter J. Turnbaugh & Ruth E. Ley & Michael A. Mahowald & Vincent Magrini & Elaine R. Mardis & Jeffrey I. Gordon, 2006. "An obesity-associated gut microbiome with increased capacity for energy harvest," Nature, Nature, vol. 444(7122), pages 1027-1031, December.
    2. Peter J. Turnbaugh & Micah Hamady & Tanya Yatsunenko & Brandi L. Cantarel & Alexis Duncan & Ruth E. Ley & Mitchell L. Sogin & William J. Jones & Bruce A. Roe & Jason P. Affourtit & Michael Egholm & Be, 2009. "A core gut microbiome in obese and lean twins," Nature, Nature, vol. 457(7228), pages 480-484, January.
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