Exercise training modifies xenometabolites in gut and circulation of lean and obese adults

Kasperek, Mikaela C; Mailing, Lucy J.; Piccolo, Brian D.; Moody, Becky; Lan, Renny S.; Gao, Xiaotian; Hernández-Saavedra, Diego; Woods, Jeffrey A.; Adams, Sean H.; Allen, John

doi:10.14814/phy2.15638

Cited by 9 publications

(12 citation statements)

References 48 publications

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“…We did not investigate the mechanism underlying the training-induced increase in aromatic lactic acids. However, increases in faecal concentrations have previously been reported for PLA [47], ILA and HPLA [48] in subjects with obesity participating in endurance exercise interventions. This points towards a contribution of the gut microbiome, which is well-known to be affected by physical exercise [47, 49, 50].…”

Section: Discussionmentioning

confidence: 99%

“…This points towards a contribution of the gut microbiome, which is well-known to be affected by physical exercise [47, 49, 50]. Interestingly, a recent study found that serum ILA and HPLA were increased in both lean and obese subjects following an exercise intervention, whereas faecal levels were increased in the obese cohort only [48]. This suggests that exercise may have diverging effects depending on the obesity status.…”

Section: Discussionmentioning

confidence: 99%

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Phenyllactic Acid is Physiologically Released from Skeletal Muscle and Contributes to the Beneficial Effects of Physical Exercise in Humans

Hoene,

Zhao,

et al. 2024

Preprint

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Methods We studied acute exercise- and training-induced changes in plasma metabolites in sedentary subjects with overweight (8 male, 14 female) participating in an eight-week supervised training program flanked by two acute endurance exercise sessions. Plasma metabolites were quantified using LC- and CE-MS. In a separate study (n=9 lean males), we assessed metabolite fluxes over the leg using arterial and venous catheters. Functional analyses were performed in primary blood mononuclear cells (PBMCs) stimulated with lipopolysaccharide (LPS) or the saturated fatty acid palmitate. Results The amino acid breakdown products 3-phenyllactic acid (PLA), 4-hydroxyphenyllactic acid and indolelactic acid were increased after both acute exercise and training. All three aromatic lactic acids, which so far mainly received attention as bacterial metabolites, exhibited an efflux from the leg. PLA showed the largest increase after both acute exercise and training, of 57% and 20% respectively. The magnitude of the acute exercise-induced increase in PLA correlated with a decrease in subcutaneous adipose tissue volume and an improvement in insulin sensitivity over the course of the intervention. Furthermore, both isomers, D and L-PLA, counteracted inflammatory cytokine production in PBMCs. Conclusions/interpretation Our findings indicate that PLA is physiologically released from skeletal muscle and can contribute to the anti-inflammatory effects of exercise as well as to individual difference in the response to lifestyle interventions in humans. PLA and potentially, aromatic lactic acids in general may be particularly relevant metabolic regulators because they can be produced both endogenously and by the microbiome.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Phenyllactic Acid is Physiologically Released from Skeletal Muscle and Contributes to the Beneficial Effects of Physical Exercise in Humans

Hoene,

Zhao,

et al. 2024

Preprint

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“…As mentioned above, acute exercise is reported to increase several microbially derived xenometabolites (Grapov et al., 2019 ). Recent findings suggest that 6 weeks of aerobic exercise training modifies xenometabolites in the gut and circulation of lean and obese humans in a physiologically relevant manner (Kasperek et al., 2023 ). Regarding very short‐term exercise, several significant changes in plasma concentrations of metabolites known to be partially or fully derived from microbial metabolism were reported following a 4‐day cross‐country ski march (Karl et al., 2017 ).…”

Section: Gaps In Knowledge and Future Directionsmentioning

confidence: 99%

Gut check: Unveiling the influence of acute exercise on the gut microbiota

Grosicki,

Langan,

Bagley

et al. 2023

Experimental Physiology

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The human gastrointestinal microbiota and its unique metabolites regulate a diverse array of physiological processes with substantial implications for human health and performance. Chronic exercise training positively modulates the gut microbiota and its metabolic output. The benefits of chronic exercise for the gut microbiota may be influenced by acute changes in microbial community structure and function that follow a single exercise bout (i.e., acute exercise). Thus, an improved understanding of changes in the gut microbiota that occur with acute exercise could aid in the development of evidence‐based exercise training strategies to target the gut microbiota more effectively. In this review, we provide a comprehensive summary of the existing literature on the acute and very short‐term (<3 weeks) exercise responses of the gut microbiota and faecal metabolites in humans. We conclude by highlighting gaps in the literature and providing recommendations for future research in this area.New Findings What is the topic of this review? The chronic benefits of exercise for the gut microbiota are likely influenced by acute changes in microbial community structure and function that follow a single exercise bout. This review provides a summary of the existing literature on acute exercise responses of the gut microbiota and its metabolic output in humans. What advances does it highlight? Acute aerobic exercise appears to have limited effects on diversity of the gut microbiota, variable effects on specific microbial taxa, and numerous effects on the metabolic activity of gut microbes with possible implications for host health and performance.

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“…Previous studies have demonstrated that exercise can modulate the composition and diversity of the intestinal microbes, as well as its metabolites and functions 102 . In addition, the intestinal microbes may also affect exercise-induced inflammation, oxidative stress, muscle damage, and immune responses 103 . In a recent study, swimming exercise has been shown to improve depressive-like behavior and boost immunity through its anti-inflammatory effects, as well as by restoring the balance of gut bacteria, such as Escherichia coli and Lactobacilli 104 .…”

Section: Behavioral Adjustmentmentioning

confidence: 99%

A comprehensive perspective on the interaction between gut microbiota and COVID-19 vaccines

Hong

Lan

et al. 2023

Gut Microbes

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The efficacy of COVID-19 vaccines varies between individuals and populations, and the reasons for this are still not fully understood. Recent clinical studies and animal models have indicated that the gut microbiota may influence the immunogenicity of the vaccine and, thus, its effectiveness. This suggests that there is a bidirectional relationship between the gut microbiota and the COVID-19 vaccine, with the varying components of the microbiota either enhancing or reducing the vaccine’s efficacy. To put an end to the spread of the COVID-19 pandemic, the necessity of vaccines that create powerful and long-term immunity is now more important than ever, and understanding the role of the gut microbiota in this process is essential. Conversely, COVID-19 vaccines also have a significant effect on the gut microbiota, decreasing its total number of organisms and the variety of species present. In this Review, we analyze the evidence that suggesting an interaction between the gut microbiota and COVID-19 vaccine effectiveness, consider the immunological mechanisms that may be responsible for this connection, and explore the possibility of using gut microbiota-focused interventions to improve the efficacy of COVID-19 vaccines.

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Exercise training modifies xenometabolites in gut and circulation of lean and obese adults

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 9 publications

References 48 publications

Phenyllactic Acid is Physiologically Released from Skeletal Muscle and Contributes to the Beneficial Effects of Physical Exercise in Humans

Phenyllactic Acid is Physiologically Released from Skeletal Muscle and Contributes to the Beneficial Effects of Physical Exercise in Humans

Gut check: Unveiling the influence of acute exercise on the gut microbiota

A comprehensive perspective on the interaction between gut microbiota and COVID-19 vaccines

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