Exercise Prevents Weight Gain and Alters the Gut Microbiota in a Mouse Model of High Fat Diet-Induced Obesity

Evans, Christian C.; LePard, Kathy J.; Kwak, Jeff W.; Stancukas, Mary C.; Laskowski, Samantha; Dougherty, Joseph; Moulton, Laura; Glawe, Adam; Wang, Yunwei; Leone, Vanessa; Antonopoulos, Dionysios A.; Smith, Dan; Chang, Eugene B.; Ciancio, Mae J.

doi:10.1371/journal.pone.0092193

Exercise Prevents Weight Gain and Alters the Gut Microbiota in a Mouse Model of High Fat Diet-Induced Obesity

Journal Article · Wed Mar 26 00:00:00 EDT 2014 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0092193· OSTI ID:1627686

Evans, Christian C. ^[1]; LePard, Kathy J. ^[2]; Kwak, Jeff W. ^[2]; Stancukas, Mary C. ^[2]; Laskowski, Samantha ^[2]; Dougherty, Joseph ^[2]; Moulton, Laura ^[2]; Glawe, Adam ^[2]; Wang, Yunwei ^[3]; Leone, Vanessa ^[3]; Antonopoulos, Dionysios A. ^[4]; Smith, Dan ^[4]; Chang, Eugene B. ^[3]; Ciancio, Mae J. ^[2]

Midwestern University, Downers Grove, IL (United States); DOE/OSTI
Midwestern University, Downers Grove, IL (United States)
University of Chicago, IL (United States)
Argonne National Laboratory (ANL), Argonne, IL (United States). Institute for Genomics and Systems Biology

Diet-induced obesity (DIO) is a significant health concern which has been linked to structural and functional changes in the gut microbiota. Exercise (Ex) is effective in preventing obesity, but whether Ex alters the gut microbiota during development with high fat (HF) feeding is unknown. Determine the effects of voluntary Ex on the gastrointestinal microbiota in LF-fed mice and in HF-DIO. Male C57BL/6 littermates (5 weeks) were distributed equally into 4 groups: low fat (LF) sedentary (Sed) LF/Sed, LF/ Ex, HF/Sed and HF/Ex. Mice were individually housed and LF/Ex and HF/Ex cages were equipped with a wheel and odometer to record Ex. Fecal samples were collected at baseline, 6 weeks and 12 weeks and used for bacterial DNA isolation. DNA was subjected both to quantitative PCR using primers specific to the 16S rRNA encoding genes for Bacteroidetes and Firmicutes and to sequencing for lower taxonomic identification using the Illumina MiSeq platform. Data were analyzed using a one or two-way ANOVA or Pearson correlation. HF diet resulted in significantly greater body weight and adiposity as well as decreased glucose tolerance that were prevented by voluntary Ex (p<0.05). Visualization of Unifrac distance data with principal coordinates analysis indicated clustering by both diet and Ex at week 12. Sequencing demonstrated Ex-induced changes in the percentage of major bacterial phyla at 12 weeks. A correlation between total Ex distance and the ΔCt Bacteroidetes: ΔCt Firmicutes ratio from qPCR demonstrated a significant inverse correlation (r² = 0.35, p = 0.043). Conclusion: Ex induces a unique shift in the gut microbiota that is different from dietary effects. Microbiota changes may play a role in Ex prevention of HF-DIO.

View Accepted Manuscript (DOE)

Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: Kenneth A. Suarez Summer Research Fellowship; Midwestern University; National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER); University of Chicago

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1627686

Journal Information:: PLoS ONE, Journal Name: PLoS ONE Journal Issue: 3 Vol. 9; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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The combination of sport and sport-specific diet is associated with characteristics of gut microbiota: an observational study Jang, Lae-Guen; Choi, Geunhoon; Kim, Sung-Woo Journal of the International Society of Sports Nutrition, Vol. 16, Issue 1 https://doi.org/10.1186/s12970-019-0290-y	journal	May 2019
Dietary silver nanoparticles can disturb the gut microbiota in mice van den Brule, Sybille; Ambroise, Jérôme; Lecloux, Hélène Particle and Fibre Toxicology, Vol. 13, Issue 1 https://doi.org/10.1186/s12989-016-0149-1	journal	December 2015
Genomic characterization of the uncultured Bacteroidales family S24-7 inhabiting the guts of homeothermic animals Ormerod, Kate L.; Wood, David L. A.; Lachner, Nancy Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0181-2	journal	July 2016
(Dis)Trust your gut: the gut microbiome in age-related inflammation, health, and disease Buford, Thomas W. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0296-0	journal	July 2017
High-fat diet reduces the level of secretory immunoglobulin A coating of commensal gut microbiota Muhomah, Teresia Aluoch; Nishino, Naoki; Katsumata, Emiko Bioscience of Microbiota, Food and Health, Vol. 38, Issue 2 https://doi.org/10.12938/bmfh.18-027	journal	January 2019
Physical Activity Differentially Affects the Cecal Microbiota of Ovariectomized Female Rats Selectively Bred for High and Low Aerobic Capacity Liu, Tzu-Wen; Park, Young-Min; Holscher, Hannah D. PLOS ONE, Vol. 10, Issue 8 https://doi.org/10.1371/journal.pone.0136150	journal	August 2015
Changes in Gut and Plasma Microbiome following Exercise Challenge in Myalgic Encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS) Shukla, Sanjay K.; Cook, Dane; Meyer, Jacob PLOS ONE, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pone.0145453	journal	December 2015
The Gut Microbiome Is Altered in a Letrozole-Induced Mouse Model of Polycystic Ovary Syndrome Kelley, Scott T.; Skarra, Danalea V.; Rivera, Alissa J. PLOS ONE, Vol. 11, Issue 1 https://doi.org/10.1371/journal.pone.0146509	journal	January 2016
The Effect of Diet and Exercise on Intestinal Integrity and Microbial Diversity in Mice Campbell, Sara C.; Wisniewski, Paul J.; Noji, Michael PLOS ONE, Vol. 11, Issue 3 https://doi.org/10.1371/journal.pone.0150502	journal	March 2016
Intense Exercise and Aerobic Conditioning Associated with Chromium or L-Carnitine Supplementation Modified the Fecal Microbiota of Fillies Almeida, Maria Luiza Mendes de; Feringer, Walter Heinz; Carvalho, Júlia Ribeiro Garcia PLOS ONE, Vol. 11, Issue 12 https://doi.org/10.1371/journal.pone.0167108	journal	December 2016
High fat diet alters gut microbiota but not spatial working memory in early middle-aged Sprague Dawley rats Deshpande, Nikita Girish; Saxena, Juhi; Pesaresi, Tristan G. PLOS ONE, Vol. 14, Issue 5 https://doi.org/10.1371/journal.pone.0217553	journal	May 2019
Comprehensive amelioration of high-fat diet-induced metabolic dysfunctions through activation of the PGC-1α pathway by probiotics treatment in mice Kwon, Jeonghyeon; Kim, Bobae; Lee, Chungho PLOS ONE, Vol. 15, Issue 2 https://doi.org/10.1371/journal.pone.0228932	journal	February 2020
The impact of exercise training and resveratrol supplementation on gut microbiota composition in high-fat diet fed mice Brandt, Nina; Kotowska, Dorota; Kristensen, Caroline M. Physiological Reports, Vol. 6, Issue 20 https://doi.org/10.14814/phy2.13881	journal	October 2018
Preventive Antibiotic Treatment Increases Neonatal Chicks Susceptibility to Salmonella Infection Via Disrupting Gut Microbiota and Linoleic Acid Metabolism Mei, Xueran; Ma, Boheng; Zhai, Xiwen Europe PMC https://doi.org/10.21203/rs.3.rs-77489/v1	journal	September 2020
Role of GDF15 in active lifestyle induced metabolic adaptations and acute exercise response in mice Gil, Carla Igual; Ost, Mario; Kasch, Juliane Universität Potsdam https://doi.org/10.25932/publishup-46054	text	January 2021
Impacts of Diet and Exercise on Maternal Gut Microbiota Are Transferred to Offspring Bhagavata Srinivasan, Shyam Prakaash; Raipuria, Mukesh; Bahari, Hasnah Frontiers in Endocrinology, Vol. 9 https://doi.org/10.3389/fendo.2018.00716	journal	November 2018
Obesity: More Than an Inflammatory, an Infectious Disease? Leocádio, Paola C. L.; Oriá, Reinaldo B.; Crespo-Lopez, Maria Elena Frontiers in Immunology, Vol. 10 https://doi.org/10.3389/fimmu.2019.03092	journal	January 2020
Human Gut Microbiota: Toward an Ecology of Disease Selber-Hnatiw, Susannah; Rukundo, Belise; Ahmadi, Masoumeh Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01265	journal	July 2017
Response of Gut Microbiota to Metabolite Changes Induced by Endurance Exercise Zhao, Xia; Zhang, Zhujun; Hu, Bin Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.00765	journal	April 2018
The Gut Microbiome on a Periodized Low-Protein Diet Is Associated With Improved Metabolic Health Li, Zhencheng; Rasmussen, Torben Sølbeck; Rasmussen, Mette Line Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.00709	journal	April 2019
A Review of the Role of the Gut Microbiome in Personalized Sports Nutrition Hughes, Riley L. Frontiers in Nutrition, Vol. 6 https://doi.org/10.3389/fnut.2019.00191	journal	January 2020
Gut Microbiota Modification: Another Piece in the Puzzle of the Benefits of Physical Exercise in Health? Cerdá, Begoña; Pérez, Margarita; Pérez-Santiago, Jennifer D. Frontiers in Physiology, Vol. 7 https://doi.org/10.3389/fphys.2016.00051	journal	February 2016
Host-Microbiome Interaction and Cancer: Potential Application in Precision Medicine Contreras, Alejandra V.; Cocom-Chan, Benjamin; Hernandez-Montes, Georgina Frontiers in Physiology, Vol. 7 https://doi.org/10.3389/fphys.2016.00606	journal	December 2016
Multi-Level Integration of Environmentally Perturbed Internal Phenotypes Reveals Key Points of Connectivity between Them Benis, Nirupama; Kar, Soumya K.; Martins dos Santos, Vitor A. P. Frontiers in Physiology, Vol. 8 https://doi.org/10.3389/fphys.2017.00388	journal	June 2017
TRIM31 Deficiency Is Associated with Impaired Glucose Metabolism and Disrupted Gut Microbiota in Mice Cheng, Jing; Xue, Fei; Zhang, Meng Frontiers in Physiology, Vol. 9 https://doi.org/10.3389/fphys.2018.00024	journal	February 2018
Intestinal Microbiota Modulation in Obesity-Related Non-alcoholic Fatty Liver Disease Porras, David; Nistal, Esther; Martínez-Flórez, Susana Frontiers in Physiology, Vol. 9 https://doi.org/10.3389/fphys.2018.01813	journal	December 2018
Physiological and Biochemical Effects of Intrinsically High and Low Exercise Capacities Through Multiomics Approaches Tung, Yu-Tang; Hsu, Yi-Ju; Liao, Chen-Chung Frontiers in Physiology, Vol. 10 https://doi.org/10.3389/fphys.2019.01201	journal	September 2019
Effects of Antidiabetic Drugs on Gut Microbiota Composition Montandon, Sophie; Jornayvaz, François Genes, Vol. 8, Issue 10 https://doi.org/10.3390/genes8100250	journal	September 2017
Toxicity, Pharmacokinetics, and Gut Microbiome of Oral Administration of Sesterterpene MHO7 Derived from a Marine Fungus Tian, Wei; Yang, Liang; Wu, Di Marine Drugs, Vol. 17, Issue 12 https://doi.org/10.3390/md17120667	journal	November 2019
The Role of Gut Microbiota in Intestinal Inflammation with Respect to Diet and Extrinsic Stressors Lobionda, Stefani; Sittipo, Panida; Kwon, Hyog Young Microorganisms, Vol. 7, Issue 8 https://doi.org/10.3390/microorganisms7080271	journal	August 2019
Limited Effects of Low-to-Moderate Aerobic Exercise on the Gut Microbiota of Mice Subjected to a High-Fat Diet Ribeiro, Filipe M.; Ribeiro, Camila F. A.; G., Ana Cláudia M. Nutrients, Vol. 11, Issue 1 https://doi.org/10.3390/nu11010149	journal	January 2019
Gut–Joint Axis: The Role of Physical Exercise on Gut Microbiota Modulation in Older People with Osteoarthritis de Sire, Alessandro; de Sire, Roberto; Petito, Valentina Nutrients, Vol. 12, Issue 2 https://doi.org/10.3390/nu12020574	journal	February 2020
Aging Gut Microbiota at the Cross-Road between Nutrition, Physical Frailty, and Sarcopenia: Is There a Gut–Muscle Axis? Ticinesi, Andrea; Lauretani, Fulvio; Milani, Christian Nutrients, Vol. 9, Issue 12 https://doi.org/10.3390/nu9121303	journal	November 2017
Additional file 1 of Dynamic distribution of gut microbiota in meat rabbits at different growth stages and relationship with average daily gain (ADG) Fang, Shaoming; Chen, Xuan; Pan, Jiahua figshare https://doi.org/10.6084/m9.figshare.12308063	dataset	January 2020
Additional file 2 of Dynamic distribution of gut microbiota in meat rabbits at different growth stages and relationship with average daily gain (ADG) Fang, Shaoming; Chen, Xuan; Pan, Jiahua figshare https://doi.org/10.6084/m9.figshare.12308072	dataset	January 2020
Bidirectional interactions between indomethacin and the murine intestinal microbiota Liang, Xue; Bittinger, Kyle; Li, Xuanwen eLife, Vol. 4 https://doi.org/10.7554/elife.08973	journal	December 2015
Intestinal Microbiota Contributes to Energy Balance, Metabolic Inflammation, and Insulin Resistance in Obesity Cavallari, Joseph F.; Schertzer, Jonathan D. Journal of Obesity & Metabolic Syndrome, Vol. 26, Issue 3 https://doi.org/10.7570/jomes.2017.26.3.161	journal	September 2017
Linking microbiota and respiratory disease Hauptmann, Matthias; Schaible, Ulrich E. FEBS Letters, Vol. 590, Issue 21 https://doi.org/10.1002/1873-3468.12421	journal	October 2016
The Intestinal Microbiome in Bariatric Surgery Patients: Gut Microbes and Bariatric Surgery Peat, Christine M.; Kleiman, Susan C.; Bulik, Cynthia M. European Eating Disorders Review, Vol. 23, Issue 6 https://doi.org/10.1002/erv.2400	journal	October 2015
Exercise Decreases Marrow Adipose Tissue Through ß-Oxidation in Obese Running Mice: EXERCISE DECREASES MAT IN OBESE MICE Styner, Maya; Pagnotti, Gabriel M.; McGrath, Cody Journal of Bone and Mineral Research, Vol. 32, Issue 8 https://doi.org/10.1002/jbmr.3159	journal	May 2017
Fungi as Part of the Microbiota and Interactions with Intestinal Bacteria Kapitan, Mario; Niemiec, M. Joanna; Steimle, Alexander Fungal Physiology and Immunopathogenesis https://doi.org/10.1007/82_2018_117	book	January 2018
Systematic review assessing the effectiveness of dietary intervention on gut microbiota in adults with type 2 diabetes Houghton, David; Hardy, Timothy; Stewart, Christopher Diabetologia, Vol. 61, Issue 8 https://doi.org/10.1007/s00125-018-4632-0	journal	May 2018
Relationship between gut microbiota, probiotics, and type 2 diabetes mellitus Salgaço, Mateus Kawata; Oliveira, Liliane Garcia Segura; Costa, Giselle Nobre Applied Microbiology and Biotechnology, Vol. 103, Issue 23-24 https://doi.org/10.1007/s00253-019-10156-y	journal	October 2019
Characteristics of fecal microbiota in non-alcoholic fatty liver disease patients Li, Fan; Sun, Gang; Wang, Zikai Science China Life Sciences, Vol. 61, Issue 7 https://doi.org/10.1007/s11427-017-9303-9	journal	June 2018
Short Term High Fat Diet Induces Obesity-Enhancing Changes in Mouse Gut Microbiota That are Partially Reversed by Cessation of the High Fat Diet Shang, Yue; Khafipour, Ehsan; Derakhshani, Hooman Lipids, Vol. 52, Issue 6 https://doi.org/10.1007/s11745-017-4253-2	journal	April 2017
The Association between Objectively Measured Physical Activity and the Gut Microbiome among Older Community Dwelling Men Langsetmo, Lisa; Johnson, A.; Demmer, R. T. The journal of nutrition, health & aging, Vol. 23, Issue 6 https://doi.org/10.1007/s12603-019-1194-x	journal	April 2019
Metabolic Adaptations to Exercise Training Liu, Sujuan; Niu, Yanmei; Fu, Li Journal of Science in Sport and Exercise, Vol. 2, Issue 1 https://doi.org/10.1007/s42978-019-0018-3	journal	July 2019
Exercise and gut immune function: evidence of alterations in colon immune cell homeostasis and microbiome characteristics with exercise training Cook, Marc D.; Allen, Jacob M.; Pence, Brandt D. Immunology and Cell Biology, Vol. 94, Issue 2 https://doi.org/10.1038/icb.2015.108	journal	December 2015
Early‐life exercise may promote lasting brain and metabolic health through gut bacterial metabolites Mika, Agnieszka; Fleshner, Monika Immunology & Cell Biology, Vol. 94, Issue 2 https://doi.org/10.1038/icb.2015.113	journal	January 2016
Enrichment of the lung microbiome with gut bacteria in sepsis and the acute respiratory distress syndrome Dickson, Robert P.; Singer, Benjamin H.; Newstead, Michael W. Nature Microbiology, Vol. 1, Issue 10 https://doi.org/10.1038/nmicrobiol.2016.113	journal	July 2016
The role of the gut microbiota in NAFLD Leung, Christopher; Rivera, Leni; Furness, John B. Nature Reviews Gastroenterology & Hepatology, Vol. 13, Issue 7 https://doi.org/10.1038/nrgastro.2016.85	journal	June 2016
Effects of the captive and wild environment on diversity of the gut microbiome of deer mice (Peromyscus maniculatus) Schmidt, Elliott; Mykytczuk, Nadia; Schulte-Hostedde, Albrecht I. The ISME Journal, Vol. 13, Issue 5 https://doi.org/10.1038/s41396-019-0345-8	journal	January 2019
An automated Raman-based platform for the sorting of live cells by functional properties Lee, Kang Soo; Palatinszky, Márton; Pereira, Fátima C. Nature Microbiology, Vol. 4, Issue 6 https://doi.org/10.1038/s41564-019-0394-9	journal	March 2019
Anti-diabetic Effects of Clostridium butyricum CGMCC0313.1 through Promoting the Growth of Gut Butyrate-producing Bacteria in Type 2 Diabetic Mice Jia, Lingling; Li, Dongyao; Feng, Ninghan Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/s41598-017-07335-0	journal	August 2017
Modulation of gut microbiota by mulberry fruit polysaccharide treatment of obese diabetic db / db mice Chen, Chun; You, Li-Jun; Huang, Qiang Food & Function, Vol. 9, Issue 7 https://doi.org/10.1039/c7fo01346a	journal	January 2018
The effect of probiotics and polysaccharides on the gut microbiota composition and function of weaned rats Wang, Mengxia; Chen, Yongxiong; Wang, Yuanyuan Food & Function, Vol. 9, Issue 3 https://doi.org/10.1039/c7fo01507k	journal	January 2018
Diet induced maternal obesity affects offspring gut microbiota and persists into young adulthood Guo, Yanjie; Wang, Zhenling; Chen, Liang Food & Function, Vol. 9, Issue 8 https://doi.org/10.1039/c8fo00444g	journal	January 2018
Bovine α-lactalbumin hydrolysates ameliorate obesity-associated endotoxemia and inflammation in high-fat diet-fed mice through modulation of gut microbiota Li, Tiange; Gao, Jing; Du, Min Food & Function, Vol. 10, Issue 6 https://doi.org/10.1039/c8fo01967c	journal	January 2019
Beneficial effects of tea water extracts on the body weight and gut microbiota in C57BL/6J mice fed with a high-fat diet Liu, Jianhui; Hao, Wangjun; He, Zouyan Food & Function, Vol. 10, Issue 5 https://doi.org/10.1039/c8fo02051e	journal	January 2019
Anti-Inflammatory Effect of Exercise Mediated by Toll-Like Receptor Regulation in Innate Immune Cells – A Review: Anti-inflammatory effect of exercise mediated by Toll-like receptor regulation in innate immune cells Collao, Nicolas; Rada, Isabel; Francaux, Marc International Reviews of Immunology, Vol. 39, Issue 2 https://doi.org/10.1080/08830185.2019.1682569	journal	November 2019
Oral supplementation of Bifidobacterium longum strain BR-108 alters cecal microbiota by stimulating gut immune system in mice irrespectively of viability Makioka, Yuko; Tsukahara, Takamitsu; Ijichi, Tetsuo Bioscience, Biotechnology, and Biochemistry, Vol. 82, Issue 7 https://doi.org/10.1080/09168451.2018.1451738	journal	July 2018
Prenatal androgen exposure causes hypertension and gut microbiota dysbiosis Sherman, Shermel B.; Sarsour, Nadeen; Salehi, Marziyeh Gut Microbes https://doi.org/10.1080/19490976.2018.1441664	journal	February 2018
The association between gut microbiome and anthropometric measurements in Bangladesh Osborne, Gwendolyn; Wu, Fen; Yang, Liying Gut Microbes, Vol. 11, Issue 1 https://doi.org/10.1080/19490976.2019.1614394	journal	May 2019
The Gut Microbiome as a Therapeutic Target for Cognitive Impairment Sun, Yi; Baptista, Liliana C.; Roberts, Lisa M. The Journals of Gerontology: Series A, Vol. 75, Issue 7 https://doi.org/10.1093/gerona/glz281	journal	December 2019
The Effects of Captivity on the Mammalian Gut Microbiome McKenzie, Valerie J.; Song, Se Jin; Delsuc, Frédéric Integrative and Comparative Biology, Vol. 57, Issue 4 https://doi.org/10.1093/icb/icx090	journal	August 2017
Analysis of intestinal immunity and flora in a collagen-induced mouse arthritis model: differences during arthritis progression Nemoto, Nobuhito; Takeda, Yuji; Nara, Hidetoshi International Immunology, Vol. 32, Issue 1 https://doi.org/10.1093/intimm/dxz058	journal	September 2019
Linseed oil and heated linseed grain supplements have different effects on rumen bacterial community structures and fatty acid profiles in cashmere kids1 Wang, Xue; Martin, Graeme B.; Wen, Qi Journal of Animal Science, Vol. 97, Issue 5 https://doi.org/10.1093/jas/skz079	journal	March 2019
Spermidine and Voluntary Activity Exert Differential Effects on Sucrose- Compared with Fat-Induced Systemic Changes in Male Mice Schipke, Julia; Vital, Marius; Schnapper-Isl, Anke The Journal of Nutrition, Vol. 149, Issue 3 https://doi.org/10.1093/jn/nxy272	journal	February 2019
Metabolic networks of the human gut microbiota Selber-Hnatiw, Susannah; Sultana, Tarin; Tse, W. Microbiology, Vol. 166, Issue 2 https://doi.org/10.1099/mic.0.000853	journal	February 2020
Formulated diet alters gut microbiota compositions in marine fish Nibea coibor and Nibea diacanthus Li, Zhongzhen; Zhang, Xinxu; Aweya, Jude Juventus Aquaculture Research, Vol. 50, Issue 1 https://doi.org/10.1111/are.13874	journal	October 2018
Gut microbiota and obesity: An opportunity to alter obesity through faecal microbiota transplant (FMT) Lee, Patrick; Yacyshyn, Bruce R.; Yacyshyn, Mary B. Diabetes, Obesity and Metabolism, Vol. 21, Issue 3 https://doi.org/10.1111/dom.13561	journal	November 2018
Exercising the hepatobiliary-gut axis. The impact of physical activity performance Molina-Molina, Emilio; Lunardi Baccetto, Raquel; Wang, David Q. -H. European Journal of Clinical Investigation, Vol. 48, Issue 8 https://doi.org/10.1111/eci.12958	journal	June 2018
Beneficial actions of microbiota-derived tryptophan metabolites Galligan, J. J. Neurogastroenterology & Motility, Vol. 30, Issue 2 https://doi.org/10.1111/nmo.13283	journal	January 2018
Genotype and rhizobium inoculation modulate the assembly of soybean rhizobacterial communities Zhong, Yongjia; Yang, Yongqing; Liu, Peng Plant, Cell & Environment, Vol. 42, Issue 6 https://doi.org/10.1111/pce.13519	journal	February 2019
Effect of Dietary Oxalate on the Gut Microbiota of the Mammalian Herbivore Neotoma albigula Miller, Aaron W.; Oakeson, Kelly F.; Dale, Colin Applied and Environmental Microbiology, Vol. 82, Issue 9 https://doi.org/10.1128/AEM.00216-16	journal	May 2016
High-intensity exercise training increases the diversity and metabolic capacity of the mouse distal gut microbiota during diet-induced obesity Denou, Emmanuel; Marcinko, Katarina; Surette, Michael G. American Journal of Physiology-Endocrinology and Metabolism, Vol. 310, Issue 11 https://doi.org/10.1152/ajpendo.00537.2015	journal	June 2016
Gut Microbiota: Modulation of Host Physiology in Obesity Nehra, Vandana; Allen, Jacob M.; Mailing, Lucy J. Physiology, Vol. 31, Issue 5 https://doi.org/10.1152/physiol.00005.2016	journal	September 2016
Gut microbiome may contribute to insulin resistance and systemic inflammation in obese rodents: a meta-analysis Jiao, Na; Baker, Susan S.; Nugent, Colleen A. Physiological Genomics, Vol. 50, Issue 4 https://doi.org/10.1152/physiolgenomics.00114.2017	journal	April 2018
The Microbiota-Gut-Brain Axis Cryan, John F.; O'Riordan, Kenneth J.; Cowan, Caitlin S. M. Physiological Reviews, Vol. 99, Issue 4 https://doi.org/10.1152/physrev.00018.2018	journal	October 2019
The Future of Vascular Biology and Medicine Kinlay, Scott; Michel, Thomas; Leopold, Jane A. Circulation, Vol. 133, Issue 25 https://doi.org/10.1161/circulationaha.116.023513	journal	June 2016
Bacterial Dissemination to the Brain in Sepsis Singer, Benjamin H.; Dickson, Robert P.; Denstaedt, Scott J. American Journal of Respiratory and Critical Care Medicine, Vol. 197, Issue 6 https://doi.org/10.1164/rccm.201708-1559oc	journal	March 2018
Exploring the microbiome in health and disease: Implications for toxicology Scotti, Elena; Boué, Stéphanie; Sasso, Giuseppe Lo Toxicology Research and Application, Vol. 1 https://doi.org/10.1177/2397847317741884	journal	January 2017
Diet and exercise orthogonally alter the gut microbiome and reveal independent associations with anxiety and cognition Kang, Silvia S.; Jeraldo, Patricio R.; Kurti, Aishe Molecular Neurodegeneration, Vol. 9, Issue 1 https://doi.org/10.1186/1750-1326-9-36	journal	January 2014
Dynamic distribution of gut microbiota in meat rabbits at different growth stages and relationship with average daily gain (ADG) Fang, Shaoming; Chen, Xuan; Pan, Jiahua BMC Microbiology, Vol. 20, Issue 1 https://doi.org/10.1186/s12866-020-01797-5	journal	May 2020
International Society of Sports Nutrition Position Stand: Probiotics Jäger, Ralf; Mohr, Alex E.; Carpenter, Katie C. Journal of the International Society of Sports Nutrition, Vol. 16, Issue 1 https://doi.org/10.1186/s12970-019-0329-0	journal	December 2019
The obese gut microbiome across the epidemiologic transition Dugas, Lara R.; Fuller, Miles; Gilbert, Jack Emerging Themes in Epidemiology, Vol. 13, Issue 1 https://doi.org/10.1186/s12982-015-0044-5	journal	January 2016
The gut microbiome in cardio-metabolic health Hansen, Tue H.; Gøbel, Rikke J.; Hansen, Torben Genome Medicine, Vol. 7, Issue 1 https://doi.org/10.1186/s13073-015-0157-z	journal	March 2015
Cardiorespiratory fitness as a predictor of intestinal microbial diversity and distinct metagenomic functions Estaki, Mehrbod; Pither, Jason; Baumeister, Peter Microbiome, Vol. 4, Issue 1 https://doi.org/10.1186/s40168-016-0189-7	journal	August 2016
Community characteristics of the gut microbiomes of competitive cyclists Petersen, Lauren M.; Bautista, Eddy J.; Nguyen, Hoan Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0320-4	journal	August 2017
Reproductive and Behavior Dysfunction Induced by Maternal Androgen Exposure and Obesity Is Likely Not Gut Microbiome-Mediated Lindheim, Lisa; Manti, Maria; Fornes, Romina Journal of the Endocrine Society, Vol. 2, Issue 12 https://doi.org/10.1210/js.2018-00266	journal	October 2018
Beneficial effects of exercise on gut microbiota functionality and barrier integrity, and gut-liver axis crosstalk in an in vivo model of early obesity and NAFLD Carbajo-Pescador, Sara; Porras, David; García-Mediavilla, María Victoria Disease Models & Mechanisms https://doi.org/10.1242/dmm.039206	journal	January 2019
Exercise Is More Effective at Altering Gut Microbial Composition and Producing Stable Changes in Lean Mass in Juvenile versus Adult Male F344 Rats Mika, Agnieszka; Van Treuren, Will; González, Antonio PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0125889	journal	May 2015
Bacterial Composition of the Human Upper Gastrointestinal Tract Microbiome Is Dynamic and Associated with Genomic Instability in a Barrett’s Esophagus Cohort Gall, Alevtina; Fero, Jutta; McCoy, Connor PLOS ONE, Vol. 10, Issue 6 https://doi.org/10.1371/journal.pone.0129055	journal	June 2015
Alterations in Gut Microbiome Composition and Barrier Function Are Associated with Reproductive and Metabolic Defects in Women with Polycystic Ovary Syndrome (PCOS): A Pilot Study Lindheim, Lisa; Bashir, Mina; Münzker, Julia PLOS ONE, Vol. 12, Issue 1 https://doi.org/10.1371/journal.pone.0168390	journal	January 2017
Differences in gut microbiota profile between women with active lifestyle and sedentary women Bressa, Carlo; Bailén-Andrino, María; Pérez-Santiago, Jennifer PLOS ONE, Vol. 12, Issue 2 https://doi.org/10.1371/journal.pone.0171352	journal	February 2017
High intensity interval training promotes total and visceral fat mass loss in obese Zucker rats without modulating gut microbiota Maillard, Florie; Vazeille, Emilie; Sauvanet, Pierre PLOS ONE, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pone.0214660	journal	April 2019
Gut microbiota influences pathological angiogenesis in obesity‐driven choroidal neovascularization Andriessen, Elisabeth MMA; Wilson, Ariel M.; Mawambo, Gaelle EMBO Molecular Medicine, Vol. 8, Issue 12 https://doi.org/10.15252/emmm.201606531	journal	November 2016
Therapeutic Approaches to Nonalcoholic Fatty Liver Disease: Exercise Intervention and Related Mechanisms Takahashi, Hirokazu; Kotani, Kazuhiko; Tanaka, Kenichi Frontiers in Endocrinology, Vol. 9 https://doi.org/10.3389/fendo.2018.00588	journal	October 2018
The Bacteriophage EF-P29 Efficiently Protects against Lethal Vancomycin-Resistant Enterococcus faecalis and Alleviates Gut Microbiota Imbalance in a Murine Bacteremia Model Cheng, Mengjun; Liang, Jiaming; Zhang, Yufeng Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.00837	journal	May 2017
Effects of Psychological, Environmental and Physical Stressors on the Gut Microbiota Karl, J. Philip; Hatch, Adrienne M.; Arcidiacono, Steven M. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.02013	journal	September 2018
Preventive Effect of Spontaneous Physical Activity on the Gut-Adipose Tissue in a Mouse Model That Mimics Crohn’s Disease Susceptibility Maillard, Florie; Vazeille, Emilie; Sauvanet, Pierre Cells, Vol. 8, Issue 1 https://doi.org/10.3390/cells8010033	journal	January 2019
Gut Microbiota and Lifestyle Interventions in NAFLD Houghton, David; Stewart, Christopher; Day, Christopher International Journal of Molecular Sciences, Vol. 17, Issue 4 https://doi.org/10.3390/ijms17040447	journal	March 2016
Mutual Interactions among Exercise, Sport Supplements and Microbiota Donati Zeppa, Sabrina; Agostini, Deborah; Gervasi, Marco Nutrients, Vol. 12, Issue 1 https://doi.org/10.3390/nu12010017	journal	December 2019
Exercise training-induced changes in the gut microbiota of Standardbred racehorses Janabi, A. H. D.; Biddle, A. S.; Klein, D. Comparative Exercise Physiology, Vol. 12, Issue 3 https://doi.org/10.3920/cep160015	journal	September 2016
Bidirectional interactions between indomethacin and the murine intestinal microbiota Liang, Xue; Bittinger, Kyle; Li, Xuanwen eLife, Vol. 4 https://doi.org/10.7554/eLife.08973	journal	December 2015

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Dietary mung bean protein reduces high-fat diet-induced weight gain by modulating host bile acid metabolism in a gut microbiota-dependent manner

Journal Article · Sun Jul 15 00:00:00 EDT 2018 · Biochemical and Biophysical Research Communications · OSTI ID:23125056

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59 BASIC BIOLOGICAL SCIENCES
adipose tissue
body weight
diet
fats
gut bacteria
mouse models
obesity
polymerase chain reaction

Exercise Prevents Weight Gain and Alters the Gut Microbiota in a Mouse Model of High Fat Diet-Induced Obesity

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