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The Effect of Athletes' Probiotic Intake May Depend on Protein and Dietary nutrients Article The Effect of Athletes’ Probiotic Intake May Depend on Protein and Dietary Fiber Intake Joy Son 1, Lae-Guen Jang 1, Byung-Yong Kim 2, Sunghee Lee 3 and Hyon Park 1,* 1 Exercise Nutrition & Biochemistry Lab., KyungHee University, Yongin 17104, Korea; [email protected] (J.S.); [email protected] (L.-G.J.) 2 ChunLab, Inc., Seocho-gu, Seoul 06725, Korea; [email protected] 3 Research Lab., Ildong Pharmaceutical Co., Ltd., Hwaseong 18449, Korea; [email protected] * Correspondence: [email protected] Received: 30 August 2020; Accepted: 22 September 2020; Published: 25 September 2020 Abstract: Studies investigating exercise-induced gut microbiota have reported that people who exercise regularly have a healthy gut microbial environment compared with sedentary individuals. In contrast, recent studies have shown that high protein intake without dietary fiber not only offsets the positive effect of exercise on gut microbiota but also significantly lowers the relative abundance of beneficial bacteria. In this study, to resolve this conundrum and find the root cause, we decided to narrow down subjects according to diet. Almost all of the studies had subjects on an ad libitum diet, however, we wanted subjects on a simplified diet. Bodybuilders who consumed an extremely high-protein/low-carbohydrate diet were randomly assigned to a probiotics intake group (n = 8) and a placebo group (n = 7) to find the intervention effect. Probiotics, comprising Lactobacillus acidophilus, L. casei, L. helveticus, and Bifidobacterium bifidum, were consumed for 60 days. As a result, supplement intake did not lead to a positive effect on the gut microbial environment or concentration of short-chain fatty acids (SCFAs). It has been shown that probiotic intake is not as effective as ergogenic aids for athletes such as bodybuilders with extreme dietary regimens, especially protein and dietary fiber. To clarify the influence of nutrition-related factors that affect the gut microbial environment, we divided the bodybuilders (n = 28) into groups according to their protein and dietary fiber intake and compared their gut microbial environment with that of sedentary male subjects (n = 15). Based on sedentary Korean recommended dietary allowance (KRDA), the bodybuilders0 intake of protein and dietary fiber was categorized into low, proper, and excessive groups, as follows: high-protein/restricted dietary fiber (n = 12), high-protein/adequate dietary fiber (n = 10), or adequate protein/restricted dietary fiber (n = 6). We found no significant differences in gut microbial diversity or beneficial bacteria between the high-protein/restricted dietary fiber and the healthy sedentary groups. However, when either protein or dietary fiber intake met the KRDA, gut microbial diversity and the relative abundance of beneficial bacteria showed significant differences to those of healthy sedentary subjects. These results suggest that the positive effect of exercise on gut microbiota is dependent on protein and dietary fiber intake. The results also suggest that the question of adequate nutrition should be addressed before supplementation with probiotics to derive complete benefits from the intervention. Keywords: gut microbiota; athletes; bodybuilder; protein; dietary fiber; probiotic 1. Introduction Adequate nutritional intake, along with exercise, not only restores energy stores depleted by exercise-induced fatigue but also enhances overall fitness [1–3]. Among the various effects of exercise, the importance of altered gut microbiota has become increasingly evident because of the study of the Nutrients 2020, 12, 2947; doi:10.3390/nu12102947 www.mdpi.com/journal/nutrients Nutrients 2020, 12, 2947 2 of 13 Nutrients 2020, 12, x FOR PEER REVIEW 2 of 13 human microbiome and the emergence of various tools for genomic analysis [4,5]. Recent studies havehuman reported microbiome that factors and the underlying emergence host of fitnessvarious are tools also for associated genomic with analysis gut microbial[4,5]. Recent status studies and regulationhave reported [6–9 that]. For factors example, underlying it has host been fitness reported are also that associated the effects with of exercise gut microbial on diabetes status [and10], obesityregulation [11], [6 and–9]. cardiovascular For example, it health has been [12] reported are mediated that the via effe changescts of in exercise the gut on microbial diabetes environment, [10], obesity such[11], and as increased cardiovascular diversity health and [12] the are presence mediated of via beneficial changes bacteria.in the gut microbial In addition, environment, a recent study such byas increased Scheiman diversity et al. reported and the thatpresence the gut of beneficial microbiome bacteria. of marathon In addition, runners a recent is richer study inby the Scheiman genus et al. reported that the gut microbiome of marathon runners is richer in the genus Veillonella than that Veillonella than that of the control group, and V. atypica has been shown to improve athletes0 recovery andof the performance control group, via and lactic V. acid atypica metabolism has been [shown13]. Lactic to improve acid is athletes rapidly′ formedrecovery in and muscles performance during high-strengthvia lactic acid metabolism aerobic exercise [13]. toLactic produce acid is propionate. rapidly formed Similarly, in muscles exercise-induced during high-strength changes aerobic in the microbialexercise to community produce propionate. affect energy Similarly, metabolism, exercise immune-induced function, changes and in oxidative the microbial stress community in athletes, therebyaffect energy influencing metabolism, various immune bodily functions function, [14 and]. oxidative stress in athletes, thereby influencing variousStudies bodily on function probioticss [14] have. been devoted to improving disease status or obesity [4,11,15]. TheStudies correlation on probiotics between have obesity-related been devoted diseases to improving and changesdisease status in the or obesity gut microbiome [4,11,15]. The is well-establishedcorrelation between [4,11 obesity,15], but-related relatively diseases few studiesand changes have exploredin the gut the microbiome relationship is well between-established motor stimulation,[4,11,15], but microbial relatively diversity, few studies and have sedentary explored lifestyles the relationship [16,17]. A between recent study motor by stimulation, Jang et al. thatmicrobial targeted diversity, bodybuilders, and sedentary long-distance lifestyles runners [16,17] and. A sedentary recent study people by showed Jang et thatal. that high targeted protein consumptionbodybuilders, combined long-distance with lowrunners dietary and fiber sedentary intake o peopleffsets exercise-induced showed that high improvements protein consumption in the gut microbialcombined environment. with low dietary In addition, fiber intake the relative offsets abundanceexercise-induced of short-chain improvements fatty acid in (SCFA)-producing the gut microbial bacteriaenvironment. was significantly In addition, the lower relative in bodybuilders abundance of with short significantly-chain fatty acid higher (SCFA) protein-producing intake thanbacteria in sedentarywas significantly subjects lower and middle- in bodybu to long-distanceilders with runnerssignificantly [18]. higher However, protein in addition intake tothan these in promisingsedentary quantitativesubjects and indicators, middle- gutto long mucosal-distance colonization, runners which[18]. However, is directly inducedin addition by probiotic to these ingestion, promising is notquantitative uniform, indicators, and the eff ectivenessgut mucosal of colonization, various probiotics which is is disputed directly [induced19]. by probiotic ingestion, is not uniform,Several inand vitro the studieseffectiveness have of reported various selectiveprobiotics colonization is disputed [19] of the. intestinal epithelium by probiotic-derivedSeveral in vitro microorganisms. studies have reported This makes selective it diffi colonizationcult to analyze of the the intestinal effects of epithelium probiotics onby probiotic-derived microorganisms. This makes it difficult to analyze the effects of probiotics on athletes0 gut microbiota and SCFAs. To overcome these limitations, and to recruit subjects that are moreathletes relevant′ gut microbiota to our aims, and we SCFAs needed. To to overcome narrow our these prospective limitations, pool and of subjects.to recruit We subjects assumed that that are probioticsmore relevant may to have our di aimsfferential, we needed effects into thosenarrow who our eat prospective a specific dietpool vs. of subjects. those who We eat assumed more freely. that Withprobiotics regards may to diet,have bodybuilders differential effects were morein those suitable who eat than a thosespecific who diet practice vs. those other who sports. eat more Therefore, freely. weWith attempted regards toto identify diet, bodybuilder specific factorss were that amoreffect thesuitable microbial than community those who of practice bodybuilders other duringsports. probioticTherefore, intake we andattempted investigated to identify whether specific probiotic factors intake that may affect supplement the microbial the effects community of exercise onof gutbodybuilders microbial status,during as probiotic reported intake in many and previous investigated studies. whether We aimed probiotic to reach intake conclusions may supplement regarding the theeffects correlations of exercise between on gut exercise, microbial probiotic status, as
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