Effect of a diet rich in galactose or fructose, with or without fructooligosaccharides, on gut microbiota composition in rats

Recent studies suggest that a diet rich in sugars significantly affects the gut microbiota. Adverse metabolic effects of sugars may partly be mediated by alterations of gut microbiota and gut health parameters, but experimental evidence is lacking. Therefore, we investigated the effects of high intake of fructose or galactose, with/without fructooligosaccharides (FOS), on gut microbiota composition in rats and explored the association between gut microbiota and low-grade systemic inflammation. Sprague–Dawley rats (n = 6/group) were fed the following isocaloric diets for 12 weeks (% of the dry weight of the sugars or FOS): (1) starch (control), (2) fructose (50%), (3) galactose (50%), (4) starch+FOS (15%) (FOS control), (5) fructose (50%)+FOS (15%), (6) galactose (50%)+FOS (15%), and (7) starch+olive (negative control). Microbiota composition in the large intestinal content was determined by sequencing amplicons from the 16S rRNA gene; 341F and 805R primers were used to generate amplicons from the V3 and V4 regions. Actinobacteria, Verrucomicrobia, Tenericutes, and Cyanobacteria composition differed between diets. Bifidobacterium was significantly higher in all diet groups where FOS was included. Modest associations between gut microbiota and metabolic factors as well as with gut permeability markers were observed, but no associations between gut microbiota and inflammation markers were observed. We found no coherent effect of galactose or fructose on gut microbiota composition. Added FOS increased Bifidobacterium but did not mitigate potential adverse metabolic effects induced by the sugars. However, gut microbiota composition was associated with several metabolic factors and gut permeability markers which warrant further investigations.

[1]  G. Qin,et al.  Effects of Different Combinations of Sugar and Starch Concentrations on Ruminal Fermentation and Bacterial-Community Composition in vitro , 2021, Frontiers in Nutrition.

[2]  A. Gunenc,et al.  Antipathogenic and probiotic potential of Lactobacillus brevis strains newly isolated from Algerian artisanal cheeses , 2021, Folia Microbiologica.

[3]  A. Wolk,et al.  Effects of High Intakes of Fructose and Galactose, with or without Added Fructooligosaccharides, on Metabolic Factors, Inflammation, and Gut Integrity in a Rat Model. , 2021, Molecular nutrition & food research.

[4]  K. Śliżewska,et al.  The Role of Probiotics in Cancer Prevention , 2020, Cancers.

[5]  P. Nilsson,et al.  Gut microbiota composition in relation to intake of added sugar, sugar-sweetened beverages and artificially sweetened beverages in the Malmö Offspring Study , 2020, European Journal of Nutrition.

[6]  R. Satokari High Intake of Sugar and the Balance between Pro- and Anti-Inflammatory Gut Bacteria , 2020, Nutrients.

[7]  E. Blaak Current metabolic perspective on malnutrition in obesity: towards more subgroup-based nutritional approaches? , 2020, Proceedings of the Nutrition Society.

[8]  Shudong He,et al.  Potential prebiotic activities of soybean peptides Maillard reaction products on modulating gut microbiota to alleviate aging-related disorders in D-galactose-induced ICR mice , 2020 .

[9]  R. Rodrigues,et al.  Role of gut microbiota in type 2 diabetes pathophysiology , 2020, EBioMedicine.

[10]  D. Katzka,et al.  A decreased abundance of clostridia characterizes the gut microbiota in eosinophilic esophagitis , 2019, Physiological reports.

[11]  A. Gasbarrini,et al.  Food Components and Dietary Habits: Keys for a Healthy Gut Microbiota Composition , 2019, Nutrients.

[12]  L. Andersen,et al.  Ruminococcus gnavus bacteraemia in a patient with multiple haematological malignancies , 2019, Access microbiology.

[13]  R. Tester,et al.  Fructose, galactose and glucose - In health and disease. , 2019, Clinical nutrition ESPEN.

[14]  Qiang Xu,et al.  Dietary fructose-induced gut dysbiosis promotes mouse hippocampal neuroinflammation: a benefit of short-chain fatty acids , 2019, Microbiome.

[15]  P. Babica,et al.  Effects of cyanobacterial toxins on the human gastrointestinal tract and the mucosal innate immune system , 2019, Environmental Sciences Europe.

[16]  A. Gasbarrini,et al.  What is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases , 2019, Microorganisms.

[17]  D. Van den Bossche,et al.  Ruminococcus gnavus bacteremia, an uncommon presentation of a common member of the human gut microbiota: case report and literature review , 2018, Acta clinica Belgica.

[18]  Fei Liu,et al.  Lactobacillus helveticus KLDS1.8701 alleviates d-galactose-induced aging by regulating Nrf-2 and gut microbiota in mice. , 2018, Food & function.

[19]  H. Flint,et al.  Mechanistic Insights Into the Cross-Feeding of Ruminococcus gnavus and Ruminococcus bromii on Host and Dietary Carbohydrates , 2018, Front. Microbiol..

[20]  S. Ng,et al.  The Gut Microbiota in the Pathogenesis and Therapeutics of Inflammatory Bowel Disease , 2018, Front. Microbiol..

[21]  Wei Chen,et al.  Effects of Different Doses of Fructooligosaccharides (FOS) on the Composition of Mice Fecal Microbiota, Especially the Bifidobacterium Composition , 2018, Nutrients.

[22]  M. Do,et al.  High-Glucose or -Fructose Diet Cause Changes of the Gut Microbiota and Metabolic Disorders in Mice without Body Weight Change , 2018, Nutrients.

[23]  E. Masini,et al.  Fructose liquid and solid formulations differently affect gut integrity, microbiota composition and related liver toxicity: a comparative in vivo study. , 2018, The Journal of nutritional biochemistry.

[24]  A. Gasbarrini,et al.  Actinobacteria: A relevant minority for the maintenance of gut homeostasis. , 2018, Digestive and liver disease : official journal of the Italian Society of Gastroenterology and the Italian Association for the Study of the Liver.

[25]  L. Cheong,et al.  Tuna Oil Alleviates d-Galactose Induced Aging in Mice Accompanied by Modulating Gut Microbiota and Brain Protein Expression. , 2018, Journal of agricultural and food chemistry.

[26]  L. Cheong,et al.  Modulation of gut microbiota by dietary supplementation with tuna oil and algae oil alleviates the effects of D-galactose-induced ageing , 2018, Applied Microbiology and Biotechnology.

[27]  D. Williams,et al.  The Gastrointestinal Microbiome: A Review , 2017, Journal of veterinary internal medicine.

[28]  Qingping Wu,et al.  Prebiotic Effect of Fructooligosaccharides from Morinda officinalis on Alzheimer’s Disease in Rodent Models by Targeting the Microbiota-Gut-Brain Axis , 2017, Front. Aging Neurosci..

[29]  C. Nakatsu,et al.  Microbial Ecology along the Gastrointestinal Tract , 2017, Microbes and environments.

[30]  S. Canizales-Quinteros,et al.  Gut Microbiota in Obesity and Metabolic Abnormalities: A Matter of Composition or Functionality? , 2017, Archives of medical research.

[31]  W. Tang,et al.  Gut microbiome and its role in cardiovascular diseases , 2017, Current opinion in cardiology.

[32]  Wei Zheng,et al.  Advanced glycation end products dietary restriction effects on bacterial gut microbiota in peritoneal dialysis patients; a randomized open label controlled trial , 2017, PloS one.

[33]  Sabine Weiskirchen,et al.  Fructose: A Dietary Sugar in Crosstalk with Microbiota Contributing to the Development and Progression of Non-Alcoholic Liver Disease , 2017, Front. Immunol..

[34]  K. Śliżewska,et al.  Effects of Probiotics, Prebiotics, and Synbiotics on Human Health , 2017, Nutrients.

[35]  M. Macleod,et al.  D-galactose-induced brain ageing model: A systematic review and meta-analysis on cognitive outcomes and oxidative stress indices , 2017, PloS one.

[36]  T. Hughes,et al.  The anti-cholesterolaemic effect of a consortium of probiotics: An acute study in C57BL/6J mice , 2017, Scientific Reports.

[37]  O. Lushchak,et al.  Association between body mass index and Firmicutes/Bacteroidetes ratio in an adult Ukrainian population , 2017, BMC Microbiology.

[38]  A. Hajnal,et al.  Diet-driven microbiota dysbiosis is associated with vagal remodeling and obesity , 2017, Physiology & Behavior.

[39]  S. Bischoff,et al.  Intestinal Barrier Function and the Gut Microbiome Are Differentially Affected in Mice Fed a Western-Style Diet or Drinking Water Supplemented with Fructose. , 2017, The Journal of nutrition.

[40]  W. Liao,et al.  Influence of diet on the gut microbiome and implications for human health , 2017, Journal of Translational Medicine.

[41]  Xiaokang Wu,et al.  Probiotics may delay the progression of nonalcoholic fatty liver disease by restoring the gut microbiota structure and improving intestinal endotoxemia , 2017, Scientific Reports.

[42]  J. Cant,et al.  Of the milk sugars, galactose, but not prebiotic galacto-oligosaccharide, improves insulin sensitivity in male Sprague-Dawley rats , 2017, PloS one.

[43]  H. Holscher Dietary fiber and prebiotics and the gastrointestinal microbiota , 2017, Gut microbes.

[44]  C. Rusch,et al.  Health Benefits of Fiber Fermentation , 2017, Journal of the American College of Nutrition.

[45]  M. Stefanelli,et al.  Cyanotoxins: producing organisms, occurrence, toxicity, mechanism of action and human health toxicological risk evaluation , 2017, Archives of Toxicology.

[46]  P. Wilmes,et al.  A Dietary Fiber-Deprived Gut Microbiota Degrades the Colonic Mucus Barrier and Enhances Pathogen Susceptibility , 2016, Cell.

[47]  Ajay S. Gulati,et al.  Akkermansia muciniphila mediates negative effects of IFNγ on glucose metabolism , 2016, Nature Communications.

[48]  B. Knebelmann,et al.  Case report and literature review , 2016, Medicine.

[49]  B. Feng,et al.  Microflora Disturbance during Progression of Glucose Intolerance and Effect of Sitagliptin: An Animal Study , 2016, Journal of diabetes research.

[50]  F. Bäckhed,et al.  From Dietary Fiber to Host Physiology: Short-Chain Fatty Acids as Key Bacterial Metabolites , 2016, Cell.

[51]  K. Ebert,et al.  Fructose malabsorption , 2016, Molecular and Cellular Pediatrics.

[52]  T. Sweeney,et al.  A Review of the Effect of Obesity and Surgically Induced Weight Loss , 2016 .

[53]  Shuainan Liu,et al.  A simple and stable galactosemic cataract model for rats. , 2015, International journal of clinical and experimental medicine.

[54]  Kavita R Pandey,et al.  Probiotics, prebiotics and synbiotics- a review , 2015, Journal of Food Science and Technology.

[55]  F. Levenez,et al.  Akkermansia muciniphila and improved metabolic health during a dietary intervention in obesity: relationship with gut microbiome richness and ecology , 2015, Gut.

[56]  T. Hosaka,et al.  Bifidobacterium species lower serum glucose, increase expressions of insulin signaling proteins, and improve adipokine profile in diabetic mice. , 2015, Biomedical research.

[57]  M. Conlon,et al.  The Impact of Diet and Lifestyle on Gut Microbiota and Human Health , 2014, Nutrients.

[58]  Lawrence A. David,et al.  Diet rapidly and reproducibly alters the human gut microbiome , 2013, Nature.

[59]  Robert C. Edgar,et al.  UPARSE: highly accurate OTU sequences from microbial amplicon reads , 2013, Nature Methods.

[60]  C. Chassard,et al.  Carbohydrates and the human gut microbiota , 2013, Current opinion in clinical nutrition and metabolic care.

[61]  T. Sweeney,et al.  The human gut microbiome: a review of the effect of obesity and surgically induced weight loss. , 2013, JAMA surgery.

[62]  Lucie Geurts,et al.  Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity , 2013, Proceedings of the National Academy of Sciences.

[63]  D Raoult,et al.  Correlation between body mass index and gut concentrations of Lactobacillus reuteri, Bifidobacterium animalis, Methanobrevibacter smithii and Escherichia coli , 2013, International Journal of Obesity.

[64]  I. Martínez,et al.  Gut microbiome composition is linked to whole grain-induced immunological improvements , 2012, The ISME Journal.

[65]  Pelin Yilmaz,et al.  The SILVA ribosomal RNA gene database project: improved data processing and web-based tools , 2012, Nucleic Acids Res..

[66]  Nicholas A. Bokulich,et al.  Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing , 2012, Nature Methods.

[67]  C. Chassard,et al.  Gut microbial adaptation to dietary consumption of fructose, artificial sweeteners and sugar alcohols: implications for host–microbe interactions contributing to obesity , 2012, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[68]  R. Siebert,et al.  Microbial Exposure During Early Life Has Persistent Effects on Natural Killer T Cell Function , 2012, Science.

[69]  Richard Hansen,et al.  IBD—what role do Proteobacteria play? , 2012, Nature Reviews Gastroenterology &Hepatology.

[70]  I. Cuthill,et al.  Improving Bioscience Research Reporting: The ARRIVE Guidelines for Reporting Animal Research † , 2012, Osteoarthritis and cartilage.

[71]  J. Clemente,et al.  The Impact of the Gut Microbiota on Human Health: An Integrative View , 2012, Cell.

[72]  Steven Salzberg,et al.  BIOINFORMATICS ORIGINAL PAPER , 2004 .

[73]  R. Curi,et al.  Regulation of Inflammation by Short Chain Fatty Acids , 2011, Nutrients.

[74]  P. Sansonetti,et al.  Intestinal mucosal adherence and translocation of commensal bacteria at the early onset of type 2 diabetes: molecular mechanisms and probiotic treatment , 2011, EMBO molecular medicine.

[75]  M. Clerici,et al.  Probiotics and health: an evidence-based review. , 2011, Pharmacological research.

[76]  J. Mayberry,et al.  Fructose Malabsorption: True Condition or a Variance From Normality , 2011, Journal of clinical gastroenterology.

[77]  I. Cuthill,et al.  Reporting : The ARRIVE Guidelines for Reporting Animal Research , 2010 .

[78]  J de Lange,et al.  An evidence-based review? , 2010, Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons.

[79]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[80]  R. Ge,et al.  Activation of the AMP activated protein kinase by short-chain fatty acids is the main mechanism underlying the beneficial effect of a high fiber diet on the metabolic syndrome. , 2010, Medical hypotheses.

[81]  Pat Baird,et al.  Health benefits of dietary fiber. , 2009, Nutrition reviews.

[82]  P. Brigidi,et al.  Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. , 2008, International journal of food microbiology.

[83]  R. Bibiloni,et al.  Changes in Gut Microbiota Control Metabolic Endotoxemia-Induced Inflammation in High-Fat Diet–Induced Obesity and Diabetes in Mice , 2008, Diabetes.

[84]  J. Cummings,et al.  Carbohydrate terminology and classification , 2007, European Journal of Clinical Nutrition.

[85]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[86]  J. Buttriss,et al.  Carbohydrates and dietary fibre , 2007 .

[87]  M. Rossi,et al.  Fermentation of Fructooligosaccharides and Inulin by Bifidobacteria: a Comparative Study of Pure and Fecal Cultures , 2005, Applied and Environmental Microbiology.

[88]  S. Simpson Of Mice . . . , 2004, Science.

[89]  J. Gordon,et al.  Molecular analysis of commensal host-microbial relationships in the intestine. , 2001, Science.

[90]  J. Hautvast,et al.  Consumption of fructooligosaccharides does not favorably affect blood glucose and serum lipid concentrations in patients with type 2 diabetes. , 1999, The American journal of clinical nutrition.

[91]  G. Spindler,et al.  An Integrative View , 1992 .

[92]  H. Aynedjian,et al.  Galactose feeding causes glomerular hyperperfusion: prevention by aldose reductase inhibition. , 1989, The American journal of physiology.

[93]  Robert C. Wolpert,et al.  A Review of the , 1985 .