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

Volumn 10, Issue 5, 2015, Pages

  Mika, Agnieszka ^a   Van Treuren, Will ^b   González, Antonio ^c   Herrera, Jonathan J ^a   Knight, Rob ^c   Fleshner, Monika ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b STANFORD UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RNA 16S;

ADULT; ADULTHOOD; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTEROIDETES; BIOMECHANICS; BODY COMPOSITION; COMMUNITY STRUCTURE; EXERCISE; FIRMICUTES; GENE SEQUENCE; INTESTINE FLORA; JUVENILE; LEAN BODY WEIGHT; MALE; METABOLISM; MICROBIAL COMMUNITY; NONHUMAN; PERINATAL PERIOD; RAT; RUNNING; SPECIES COMPOSITION; TAXONOMY; ANIMAL; FISCHER 344 RAT; GASTROINTESTINAL TRACT; GENETICS; MICROBIOLOGY; PHYSIOLOGY;

ANIMALS; BODY COMPOSITION; GASTROINTESTINAL TRACT; MALE; PHYSICAL CONDITIONING, ANIMAL; RATS; RATS, INBRED F344; RNA, RIBOSOMAL, 16S;

EID: 84945167269     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0125889     Document Type: Article

References (80)

1. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005; 308: 1635-1638. PMID: 15831718
2. Hill MJ. Intestinal flora and endogenous vitamin synthesis. Eur J Cancer Prev. 1997; 6 Suppl 1: S43-45. PMID: 9167138
3. Conly JM, Stein K, Worobetz L, Rutledge-Harding S. The contribution of vitamin K2 (menaquinones) produced by the intestinal microflora to human nutritional requirements for vitamin K. Am J Gastroenterol. 1994; 89: 915-923. PMID: 8198105
4. Sommer F, Backhed F. The gut microbiota-masters of host development and physiology. Nat Rev Microbiol. 2013; 11: 227-238. doi: 10.1038/nrmicro2974 PMID: 23435359
5. Hrncir T, Stepankova R, Kozakova H, Hudcovic T, Tlaskalova-Hogenova H. Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells: studies in germ-free mice. BMC Immunol. 2008; 9: 65. doi: 10.1186/1471-2172-9-65 PMID: 18990206
6. Tlaskalova-Hogenova H, Stepankova R, Hudcovic T, Tuckova L, Cukrowska B, Lodinova-Zadnikova R, et al. Commensal bacteria (normal microflora), mucosal immunity and chronic inflammatory and autoimmune diseases. Immunol Lett. 2004; 93: 97-108. PMID: 15158604
7. Ohara Y, McCarron RM, Hoffman TT, Sugano H, Bembry J, Lenz FA, et al. Adrenergic mediation of TNF alpha-stimulated ICAM-1 expression on human brain microvascular endothelial cells. Acta Neurochir Suppl. 2000; 76: 117-120. PMID: 11449988
8. Hooper LV, Stappenbeck TS, Hong CV, Gordon JI. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol. 2003; 4: 269-273. PMID: 12548285
9. Berg RD, Garlington AW. Translocation of certain indigenous bacteria from the gastrointestinal tract to the mesenteric lymph nodes and other organs in a gnotobiotic mouse model. Infect Immun. 1979; 23: 403-411. PMID: 154474
10. Ridaura VK, Faith JJ, Rey FE, Cheng J, Duncan AE, Kau AL, et al. Gut microbiota from twins discordant for obesity modulate metabolism in mice. Science. 2013; 341: 1241214. doi: 10.1126/science.1241214 PMID: 24009397
11. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, et al. The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A. 2004; 101: 15718-15723. PMID: 15505215
12. Turnbaugh PJ, Hamady M, Yatsunenko T, Cantarel BL, Duncan A, Ley RE, et al. A core gut microbiome in obese and lean twins. Nature. 2009; 457: 480-484. doi: 10.1038/nature07540 PMID: 19043404
13. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI. An obesity-Associated gut microbiome with increased capacity for energy harvest. Nature. 2006; 444: 1027-1031. PMID: 17183312
14. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, et al. Human colonic microbiota associated with diet, obesity and weight loss. Int J Obes (Lond). 2008; 32: 1720-1724. doi: 10.1038/ijo. 2008.155 PMID: 18779823
15. Schwiertz A, Taras D, Schafer K, Beijer S, Bos NA, Donus C, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity (Silver Spring). 2010; 18: 190-195. doi: 10.1038/oby.2009.167 PMID: 19498350
16. Round JL, Mazmanian SK. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A. 2010; 107: 12204-12209. doi: 10.1073/pnas. 0909122107 PMID: 20566854
17. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science. 2011; 331: 337-341. doi: 10.1126/science. 1198469 PMID: 21205640
18. Bravo JA, Forsythe P, Chew MV, Escaravage E, Savignac HM, Dinan TG, et al. Ingestion of Lactobacillus strain regulates emotional behavior and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci U S A. 2011; 108: 16050-16055. doi: 10.1073/pnas.1102999108 PMID: 21876150
19. Messaoudi M, Lalonde R, Violle N, Javelot H, Desor D, Nejdi A, et al. Assessment of psychotropic-like properties of a probiotic formulation (Lactobacillus helveticus R0052 and Bifidobacterium longum R0175) in rats and human subjects. Br J Nutr. 2011; 105: 755-764. doi: 10.1017/S0007114510004319 PMID: 20974015
20. Rao AV, Bested AC, Beaulne TM, Katzman MA, Iorio C, Berardi JM, et al. A randomized, double-blind, placebo-controlled pilot study of a probiotic in emotional symptoms of chronic fatigue syndrome. Gut Pathog. 2009; 1: 6. doi: 10.1186/1757-4749-1-6 PMID: 19338686
21. Sudo N, Chida Y, Aiba Y, Sonoda J, Oyama N, Yu XN, et al. Postnatal microbial colonization programs the hypothalamic-pituitary-Adrenal system for stress response in mice. J Physiol. 2004; 558: 263-275. PMID: 15133062
22. Diaz Heijtz R, Wang S, Anuar F, Qian Y, Bjorkholm B, Samuelsson A, et al. Normal gut microbiota modulates brain development and behavior. Proc Natl Acad Sci U S A. 2011; 108: 3047-3052. doi: 10. 1073/pnas.1010529108 PMID: 21282636
23. Sudo N, Sawamura S, Tanaka K, Aiba Y, Kubo C, Koga Y. The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol. 1997; 159: 1739-1745. PMID: 9257835
24. Cox LM, Yamanishi S, Sohn J, Alekseyenko AV, Leung JM, Cho I, et al. Altering the intestinal microbiota during a critical developmental window has lasting metabolic consequences. Cell. 2014; 158: 705-721. doi: 10.1016/j.cell.2014.05.052 PMID: 25126780
25. Kalliomaki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008; 87: 534-538. PMID: 18326589
26. Ajslev TA, Andersen CS, Gamborg M, Sorensen TI, Jess T. Childhood overweight after establishment of the gut microbiota: the role of delivery mode, pre-pregnancy weight and early administration of antibiotics. Int J Obes (Lond). 2011; 35: 522-529. doi: 10.1038/ijo.2011.27 PMID: 21386800
27. Murphy R, Stewart AW, Braithwaite I, Beasley R, Hancox RJ, Mitchell EA, et al. Antibiotic treatment during infancy and increased body mass index in boys: an international cross-sectional study. Int J Obes (Lond). 2014; 38: 1115-1119. doi: 10.1038/ijo.2013.218 PMID: 24257411
28. Wall R, Ross RP, Ryan CA, Hussey S, Murphy B, Fitzgerald GF, et al. Role of gut microbiota in early infant development. Clin Med Pediatr. 2009; 3: 45-54. PMID: 23818794
29. O'Toole PW, Claesson MJ. Gut microbiota: Changes throughout the lifespan from infancy to elderly International Dairy Journal 2010;: 281-291.
30. Yatsunenko T, Rey FE, Manary MJ, Trehan I, Dominguez-Bello MG, Contreras M, et al. Human gut microbiome viewed across age and geography. Nature. 2012; 486: 222-227. doi: 10.1038/nature11053 PMID: 22699611
31. Palmer C, Bik EM, DiGiulio DB, Relman DA, Brown PO. Development of the human infant intestinal microbiota. PLoS Biol. 2007; 5: e177. PMID: 17594176
32. Koenig JE, Spor A, Scalfone N, Fricker AD, Stombaugh J, Knight R, et al. Succession of microbial consortia in the developing infant gut microbiome. Proc Natl Acad Sci U S A. 2011; 108 Suppl 1: 4578-4585. doi: 10.1073/pnas.1000081107 PMID: 20668239
33. Queipo-Ortuno MI, Seoane LM, Murri M, Pardo M, Gomez-Zumaquero JM, Cardona F, et al. Gut microbiota composition in male rat models under different nutritional status and physical activity and its association with serum leptin and ghrelin levels. PLoS One. 2013; 8: e65465. doi: 10.1371/journal.pone. 0065465 PMID: 23724144
34. Million M, Angelakis E, Maraninchi M, Henry M, Giorgi R, Valero R, et al. Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli. International Journal of Obesity. 2013; 37: 1460-1466. doi: 10. 1038/ijo.2013.20 PMID: 23459324
35. Matsumoto M, Inoue R, Tsukahara T, Ushida K, Chiji H, Matsubara N, et al. Voluntary running exercise alters microbiota composition and increases n-butyrate concentration in the rat cecum. Biosci Biotechnol Biochem. 2008; 72: 572-576. PMID: 18256465
36. Gao Z, Yin J, Zhang J, Ward RE, Martin RJ, Lefevre M, et al. Butyrate improves insulin sensitivity and increases energy expenditure in mice. Diabetes. 2009; 58: 1509-1517. doi: 10.2337/db08-1637 PMID: 19366864
37. Evans CC, LePard KJ, Kwak JW, Stancukas MC, Laskowski S, Dougherty J, et al. Exercise prevents weight gain and alters the gut microbiota in a mouse model of high fat diet-induced obesity. PLoS One. 2014; 9: e92193. doi: 10.1371/journal.pone.0092193 PMID: 24670791
38. Greenwood BN, Foley TE, Le TV, Strong PV, Loughridge AB, Day HE, et al. Long-term voluntary wheel running is rewarding and produces plasticity in the mesolimbic reward pathway. Behav Brain Res. 2011; 217: 354-362. doi: 10.1016/j.bbr.2010.11.005 PMID: 21070820
39. Mann PB, Jiang W, Zhu Z, Wolfe P, McTiernan A, Thompson HJ. Wheel running, skeletal muscle aerobic capacity and 1-methyl-1-nitrosourea induced mammary carcinogenesis in the rat. Carcinogenesis. 2010; 31: 1279-1283. doi: 10.1093/carcin/bgq063 PMID: 20299525
40. Speaker KJ, Cox SS, Paton MM, Serebrakian A, Maslanik T, Greenwood BN, et al. Six weeks of voluntary wheel running modulates inflammatory protein (MCP-1, IL-6, and IL-10) and DAMP (Hsp72) responses to acute stress in white adipose tissue of lean rats. Brain Behav Immun. 2014; 39: 87-98. doi: 10.1016/j.bbi.2013.10.028 PMID: 24246250
41. Greenwood BN, Fleshner M. Exercise, learned helplessness, and the stress-resistant brain. Neuromolecular Med. 2008; 10: 81-98. doi: 10.1007/s12017-008-8029-y PMID: 18300002
42. Greenwood BN, Foley TE, Burhans D, Maier SF, Fleshner M. The consequences of uncontrollable stress are sensitive to duration of prior wheel running. Brain Res. 2005; 1033: 164-178. PMID: 15694921
43. Greenwood BN, Foley TE, Day HE, Campisi J, Hammack SH, Campeau S, et al. Freewheel running prevents learned helplessness/behavioral depression: role of dorsal raphe serotonergic neurons. J Neurosci. 2003; 23: 2889-2898. PMID: 12684476
44. Greenwood BN, Loughridge AB, Sadaoui N, Christianson JP, Fleshner M. The protective effects of voluntary exercise against the behavioral consequences of uncontrollable stress persist despite an increase in anxiety following forced cessation of exercise. Behav Brain Res. 2012; 233: 314-321. doi: 10. 1016/j.bbr.2012.05.017 PMID: 22610051
45. Meijer JH, Robbers Y. Wheel running in the wild. Proc Biol Sci. 2014;281.
46. Takemoto TI, Suzuki T, Miyama T. Effects of isolation on mice in relation to age and sex. Tohoku J Exp Med. 1975; 117: 153-165. PMID: 1209605
47. Restrepo C, Armario A. Chronic stress alters pituitary-Adrenal function in prepubertal male rats. Psychoneuroendocrinology. 1987; 12: 393-398. PMID: 2829263
48. Caporaso JG, Lauber CL, Costello EK, Berg-Lyons D, Gonzalez A, Stombaugh J, et al. Moving pictures of the human microbiome. Genome Biol. 2011; 12: R50. doi: 10.1186/gb-2011-12-5-r50 PMID: 21624126
49. Maslanik T, Tannura K, Mahaffey L, Loughridge AB, Benninson L, Ursell L, et al. Commensal bacteria and MAMPs are necessary for stress-induced increases in IL-1beta and IL-18 but not IL-6, IL-10 or MCP-1. PLoS One. 2012; 7: e50636. doi: 10.1371/journal.pone.0050636 PMID: 23236381
50. Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011; 108 Suppl 1: 4516-4522. doi: 10.1073/pnas.1000080107 PMID: 20534432
51. Navas-Molina JA, Peralta-Sanchez JM, Gonzalez A, McMurdie PJ, Vazquez-Baeza Y, Xu Z, et al. Advancing our understanding of the human microbiome using QIIME. Methods Enzymol. 2013; 531: 371-444. doi: 10.1016/B978-0-12-407863-5.00019-8 PMID: 24060131
52. McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, et al. An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. ISME J. 2012; 6: 610-618. doi: 10.1038/ismej.2011.139 PMID: 22134646
53. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010; 7: 335-336. doi: 10. 1038/nmeth.f.303 PMID: 20383131
54. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010; 26: 2460-2461. doi: 10.1093/bioinformatics/btq461 PMID: 20709691
55. McMurdie PJ, Holmes S. Waste not, want not: why rarefying microbiome data is inadmissible. PLoS Comput Biol. 2014; 10: e1003531. doi: 10.1371/journal.pcbi.1003531 PMID: 24699258
56. Vazquez-Baeza Y, Pirrung M, Gonzalez A, Knight R. EMPeror: a tool for visualizing high-throughput microbial community data. Gigascience. 2013; 2: 16. doi: 10.1186/2047-217X-2-16 PMID: 24280061
57. Faith DP. Conservation evaluation and phylogenic diversity. Biological Conservation. 1992; 61: 1-10.
58. Lozupone C, Knight R. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol. 2005; 71: 8228-8235. PMID: 16332807
59. Knights D, Costello EK, Knight R. Supervised classification of human microbiota. FEMS Microbiol Rev. 2011; 35: 343-359. doi: 10.1111/j.1574-6976.2010.00251.x PMID: 21039646
60. Smith D Jr., Johnson M, Nagy T. Precision and accuracy of bioimpedance spectroscopy for determination of in vivo body composition in rats. Int J Body Compos Res. 2009; 7: 21-26. PMID: 19668348
61. Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (Methodological). 1995; 57: 289-300.
62. Clarke SF, Murphy EF, O'Sullivan O, Lucey AJ, Humphreys M, Hogan A, et al. Exercise and associated dietary extremes impact on gut microbial diversity. Gut. 2014.
63. Petriz BA, Castro AP, Almeida JA, Gomes CP, Fernandes GR, Kruger RH, et al. Exercise induction of gut microbiota modifications in obese, non-obese and hypertensive rats. BMC Genomics. 2014; 15: 511. doi: 10.1186/1471-2164-15-511 PMID: 24952588
64. Kang SS, Jeraldo PR, Kurti A, Miller ME, Cook MD, Whitlock K, et al. Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition. Mol Neurodegener. 2014; 9: 36. doi: 10.1186/1750-1326-9-36 PMID: 25217888
65. Santacruz A, Marcos A, Warnberg J, Marti A, Martin-Matillas M, Campoy C, et al. Interplay between weight loss and gut microbiota composition in overweight adolescents. Obesity (Silver Spring). 2009; 17: 1906-1915. doi: 10.1038/oby.2009.112 PMID: 19390523
66. Bercik P, Park AJ, Sinclair D, Khoshdel A, Lu J, Huang X, et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil. 2011; 23: 1132-1139. doi: 10.1111/j.1365-2982.2011.01796.x PMID: 21988661
67. Desbonnet L, Garrett L, Clarke G, Bienenstock J, Dinan TG. The probiotic Bifidobacteria infantis: An assessment of potential antidepressant properties in the rat. J Psychiatr Res. 2008; 43: 164-174. doi: 10. 1016/j.jpsychires.2008.03.009 PMID: 18456279
68. McAllan L, Skuse P, Cotter PD, O'Connor P, Cryan JF, Ross RP, et al. Protein quality and the protein to carbohydrate ratio within a high fat diet influences energy balance and the gut microbiota in C57BL/6J mice. PLoS One. 2014; 9: e88904. doi: 10.1371/journal.pone.0088904 PMID: 24520424
69. Wilson M Microbial inhabitants of humans: Their ecology and role in health and disease. Cambridge, UK: Cambridge University Press; 2005.
70. Shindo D, Matsuura T, Suzuki M. Effects of prepubertal-onset exercise on body weight changes up to middle age in rats. J Appl Physiol (1985). 2014; 116: 674-682. doi: 10.1152/japplphysiol.00405.2013 PMID: 24458753
71. Trasande L, Blustein J, Liu M, Corwin E, Cox LM, Blaser MJ. Infant antibiotic exposures and early-life body mass. Int J Obes (Lond). 2013; 37: 16-23. doi: 10.1038/ijo.2012.132 PMID: 22907693
72. Tremaroli V, Backhed F. Functional interactions between the gut microbiota and host metabolism. Nature. 2012; 489: 242-249. doi: 10.1038/nature11552 PMID: 22972297
73. Korecka A, de Wouters T, Cultrone A, Lapaque N, Pettersson S, Dore J, et al. ANGPTL4 expression induced by butyrate and rosiglitazone in human intestinal epithelial cells utilizes independent pathways. Am J Physiol Gastrointest Liver Physiol. 2013; 304: G1025-1037. doi: 10.1152/ajpgi.00293.2012 PMID: 23518684
74. Aronsson L, Huang Y, Parini P, Korach-Andre M, Hakansson J, Gustafsson JA, et al. Decreased fat storage by Lactobacillus paracasei is associated with increased levels of angiopoietin-like 4 protein (ANGPTL4). PLoS One. 2010; 5.
75. Salonen A, Lahti L, Salojarvi J, Holtrop G, Korpela K, Duncan SH, et al. Impact of diet and individual variation on intestinal microbiota composition and fermentation products in obese men. ISME J. 2014.
76. Bisgaard H, Li N, Bonnelykke K, Chawes BL, Skov T, Paludan-Muller G, et al. Reduced diversity of the intestinal microbiota during infancy is associated with increased risk of allergic disease at school age. J Allergy Clin Immunol. 2011; 128: 646-652 e641-645. doi: 10.1016/j.jaci.2011.04.060 PMID: 21782228
77. Haange SB, Oberbach A, Schlichting N, Hugenholtz F, Smidt H, von Bergen M, et al. Metaproteome analysis and molecular genetics of rat intestinal microbiota reveals section and localization resolved species distribution and enzymatic functionalities. J Proteome Res. 2012; 11: 5406-5417. doi: 10. 1021/pr3006364 PMID: 23016992
78. Stevenson JA, Box BM, Feleki V, Beaton JR. Bouts of exercise and food intake in the rat. J Appl Physiol. 1966; 21: 118-122. PMID: 5903897
79. Adolph EF. Urges to eat and drink in rats. Am J Physiol. 1947; 151: 110-125. PMID: 20271650
80. Mai V, Colbert LH, Perkins SN, Schatzkin A, Hursting SD. Intestinalmicrobiota: a potential diet-responsive prevention target in ApcMinmice.Mol Carcinog. 2007; 46: 42-48. PMID: 16929480