Intestinal microbiota and microbial metabolites are changed in a pig model fed a high-fat/low-fiber or a low-fat/high-fiber diet

PLoS ONE

Volumn 11, Issue 4, 2016, Pages

  Heinritz, Sonja N ^a   Weiss, Eva ^a   Eklund, Meike ^a   Aumiller, Tobias ^a   Louis, Sandrine ^a   Rings, Andreas ^a   Messner, Sabine ^a   Camarinha Silva, Amélia ^a   Seifert, Jana ^a   Bischoff, Stephan C ^a   Mosenthin, Rainer ^a  

^a UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; BACTERIAL DNA; BUTYRIC ACID; POLYSACCHARIDE; SHORT CHAIN FATTY ACID; BUTYRIC ACID DERIVATIVE; OLIGONUCLEOTIDE; VOLATILE FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIFIDOBACTERIUM; CARBOHYDRATE METABOLISM; DIETARY FIBER; DNA FINGERPRINTING; ENTEROBACTERIACEAE; EXPERIMENTAL MODEL; FAECALIBACTERIUM PRAUSNITZII; FATTY ACID SYNTHESIS; FECES ANALYSIS; FOOD COMPOSITION; GENE DOSAGE; INTESTINE FLORA; LACTOBACILLUS; LIPID DIET; LOW FAT DIET; MALE; MICROBIAL COMMUNITY; MICROBIAL METABOLISM; NONHUMAN; PIG; POPULATION ABUNDANCE; PREVOTELLACEAE; PROTEOMICS; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; ANIMAL; CHEMISTRY; FAECALIBACTERIUM; FECES; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; RANDOMIZATION;

ANIMALS; BIFIDOBACTERIUM; BUTYRATES; DIET, FAT-RESTRICTED; DIET, HIGH-FAT; DIETARY FIBER; DNA FINGERPRINTING; DNA, BACTERIAL; FAECALIBACTERIUM; FATTY ACIDS, VOLATILE; FECES; GASTROINTESTINAL MICROBIOME; GENE DOSAGE; LACTOBACILLUS; MALE; MODELS, ANIMAL; OLIGONUCLEOTIDES; PROTEOMICS; RANDOM ALLOCATION; REAL-TIME POLYMERASE CHAIN REACTION; SWINE;

EID: 84964681660     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0154329     Document Type: Article

References (71)

1. Heinritz SN, Mosenthin R, Weiss E. Use of pigs as a potential model for research into dietary modulation of the human gut microbiota. Nutr Res Rev. 2013; 26:191-209. doi: 10.1017/S0954422413000152 PMID: 24134811
2. Miquel S, Martin R, Rossi O, Bermudez-Humaran L, Chatel J, Sokol H, et al. Faecalibacterium prausnitzii and human intestinal health. Curr Opin Microbiol. 2013; 16:255-61. doi: 10.1016/j.mib.2013.06.003 PMID: 23831042
3. Bublitz DC, Wright PC, Bodager JR, Rasambainarivo FT, Bliska JB, Gillespie TR. Epidemiology of pathogenic enterobacteria in humans, livestock, and peridomestic rodents in rural Madagascar. PLOS ONE. 2014; 9:e101456. doi: 10.1371/journal.pone.0101456 PMID: 24983990
4. De Filippo C, Cavalieria D, Di Paola M, Ramazzotti M, Poullet JB, Massart S, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci. 2010; 107:14691-96. doi: 10.1073/pnas.1005963107 PMID: 20679230
5. Anderson JW, Baird P, Davis RH Jr, Ferreri S, Knudtson M, Koraym A, et al. Health benefits of dietary fiber. Nutr Rev. 2009; 67:188-205. doi: 10.1111/j.1753-4887.2009.00189.x PMID: 19335713
6. Fraser JR, Holmes DC. Proximate analysis of wheat flour carbohydrates. IV. -Analysis of wholemeal flour and some of its fractions. J Sci Food Agric. 1959; 10:506-12.
7. Fung KY, Cosgrove L, Lockett T, Head R, Topping DL. A review of the potential mechanisms for the lowering of colorectal oncogenesis by butyrate. Br J Nutr. 2012; 108:820-31. doi: 10.1017/ S0007114512001948 PMID: 22676885
8. Moreira APB, Texeira TFS, Ferreira AB, do Carmo Gouveia Peluzio M, de Cássia Goņalves Alfenas R. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr. 2012; 108:801-9. doi: 10.1017/S0007114512001213 PMID: 22717075
9. Damms-Machado A, Mitra S, Schollenberger AE, Kramer KM, Meile T, Königsrainer A, et al. Effects of surgical and dietary weight loss therapy for obesity on gut microbiota composition and nutrient absorption. Biomed Res Int. 2015; doi: 10.1155/2015/806248
10. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA. 2005; 102:11070-5. PMID: 16033867
11. Fava F, Gitau R, Griffin BA, Gibson GR, Tuohy KM, Lovegrove JA. The type and quantity of dietary fat and carbohydrate alter faecal microbiome and short-chain fatty acid excretion in a metabolic syndrome 'at-risk' population. Int J Obes. 2013; 37:216-23.
12. Wang M, Donovan SM. Human microbiota-associated swine: Current progress and future opportunities. ILAR J. 2015; 56:63-73. doi: 10.1093/ilar/ilv006 PMID: 25991699
13. Gonzalez LM, Moeser AJ, Blikslager AT. Porcine models of digestive disease: the future of large animal translational research. Transl Res. 2015; 166:12-27. doi: 10.1016/j.trsl.2015.01.004 PMID: 25655839
14. Nguyen TLA, Vieira-Silva S, Liston A, Raes J. How informative is the mouse for human gut microbiota research? Dis Model Mech. 2015; 8:1-16. doi: 10.1242/dmm.017400 PMID: 25561744
15. Leser TD, Amernuvor JZ, Jensen TK. Culture independent analysis of gut bacteria: the pig gastrointestinal tract microbiota revisited. Appl Environ Microbiol. 2002; 68:673-90. PMID: 11823207
16. Mikkelsen LL, Bendixen C, Jakobsen M, Jensen BB. Enumeration of bifidobacteria in gastrointestinal samples from piglets. Appl Environ Microbiol. 2003; 69:654-58. PMID: 12514055
17. Simpson PJ, Stanton C, Fitzgerald GF, Ross RP. Genomic diversity and relatedness of bifidobacteria isolated from a porcine cecum. J Bacteriol. 2003; 185:2571-81. PMID: 12670982
18. Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K. Development of a real-time PCR method for Firmicutes and Bacteroidetes in faeces and its application to quantify intestinal population of obese and lean pigs. Lett Appl Microbiol. 2008; 47:367-73. doi: 10.1111/j.1472-765X.2008.02408.x PMID: 19146523
19. Pedersen R, Ingerslev HC, Sturek M, Alloosh M, Cirera S, Christoffersen B, et al. Characterisation of gut microbiota in Ossabaw and Göttingen minipigs as models of obesity and metabolic syndrome. PLOS ONE. 2013; 8:e56612. doi: 10.1371/journal.pone.0056612 PMID: 23437186
20. Yan H, Potu R, Lu H, Vezzoni de Almeida V, Stewart T, Ragland D, et al. Dietary fat content and fiber type modulate hind gut microbial community and metabolic markers in the pig. PLOS ONE. 2013; 8: e59581. doi: 10.1371/journal.pone.0059581 PMID: 23573202
21. NRC. Nutrient Requirements of Swine. 11th rev. ed. Washington, DC: National Academies Press;2012.
22. Noblet J, Fortune H, Shi XS, Dubois S. Prediction of net energy value of feeds for growing pigs. J Anim Sci. 1994; 72:344-54. PMID: 8157519
23. Pettigrew JE, Moser RL. Fat in Swine Nutrition. In: Miller ER, Ullrey DE, Lewis AJ, editors. Swine Nutrition. Butterworth-Heineman, Stoneham, MA; 1991. p.133-45.
24. Naumann C, Basler R. Die chemische Untersuchung von Futtermitteln. VDLUFA-Methodenbuch Band III, VDLUFA-Verlag. Darmstadt: Germany; 1997.
25. Weiss E, Aumiller T, Spindler HK, Rosenfelder P, Eklund M, Witzig M, et al. Wheat and barley differently affect porcine intestinal microbiota. J Sci Food Agric. 2015; doi: 10.1002/jsfa.7340
26. Yu Z, Morrison M. Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques. 2004; 36:808-12. PMID: 15152600
27. Wagnerberger S, Spruss A, Kanuri G, Volynets V, Stahl C, Bischoff SC, et al. Toll-like receptors 1-9 are elevated in livers with fructose-induced hepatic steatosis. Br J Nutr. 2012; 107:1727-38. doi: 10. 1017/S0007114511004983 PMID: 22018861
28. Bray JR, Curtis JT. An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr.1957; 27:325-49.
29. Clarke KR, Warwick RM. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. 2nd ed. Primer-e Ltd, Plymouth Marine Laboratory, UK; 2001.
30. Anderson MJ. A new method for non-parametric multivariate analysis of variance. Austral Ecol. 2001; 26:32-46.
31. 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; 11:5406-17. doi: 10.1021/ pr3006364 PMID: 23016992
32. Jehmlich N, Schmidt F, Hartwich M, von Bergen M, Richnow HH, Vogt C. Incorporation of carbon and nitrogen atoms into proteins measured by protein-based stable isotope probing (Protein-SIP). Rapid Commun Mass Spectrom. 2008; 22:2889-97. doi: 10.1002/rcm.3684 PMID: 18727149
33. Elias JE, Haas W, Faherty BK, Gygi SP (2005) Comparative evaluation of mass spectrometry platforms used in large-scale proteomics investigations. Nat Methods 2: 667-675. PMID: 16118637
34. Wu S, Zhu Z, Fu L, Niu B, Li W. WebMGA: a customizable web server for fast metagenomic sequence analysis. BMC Genomics. 2011; 12:444. doi: 10.1186/1471-2164-12-444 PMID: 21899761
35. Bardou P, Mariette J, Escudie F, Djemiel C, Klopp C. jvenn: an interactive Venn diagram viewer. BMC Bioinformatics.2014; 15:293. doi: 10.1186/1471-2105-15-293 PMID: 25176396
36. Vizcaíno JA, Deutsch EW, Wang R, Csordas A, Reisinger F, Ríos D, et al. ProteomeXchange provides globally co-ordinated proteomics data submission and dissemination. Nature Biotechnol. 2014; 30:223-26.
37. Zijlstra JB, Beukema J, Wolthers BG, Byrne BM, Groen A, Dankert J. Pretreatment methods prior to gas chromatographic analysis of volatile fatty acids from faecal samples. Clin Chim Acta. 1977; 78:243-50. PMID: 884859
38. Kenward MG, Roger JH. Small sample inference for fixed effects from restricted maximum likelihood. Biometrics.1997; 53:983-97. PMID: 9333350
39. Winer BJ, Brown DR, Michels KM. Statistical principles in experimental design. 3rd ed. New York: McGraw-Hill; 1991.
40. Piepho HP. An algorithm for a letter-based representation of all-pairwise comparisons. J Comput Graph Stat. 2004; 13:456-66.
41. Slavin S. Fiber and Prebiotics: Mechanisms and Health Benefits. Nutrients. 2013; 5:1417-35. doi: 10. 3390/nu5041417 PMID: 23609775
42. Wang J, Sun B, Cao Y, Wang C. In vitro fermentation of xylooligosaccharides from wheat bran insoluble dietary fiber by Bifidobacteria. Carbohydr Polym. 2010; 82:419-23.
43. Loh G, Eberhard M, Brunner RM, Hennig U, Kuhla S, Kleessen B, et al. Inulin alters the intestinal microbiota and short-chain fatty acid concentrations in growing pigs regardless of their basal diet. J Nutr. 2006; 136:1198-202. PMID: 16614404
44. Hermes RG, Molist F, Ywazaki M, Nofrarías M, Gomez de Segura A, Gasa J, et al. Effect of dietary level of protein and fiber on the productive performance and health status of pigs. J Anim Sci. 2009; 87:3569-77. doi: 10.2527/jas.2008-1241 PMID: 19648494
45. Pieper R, Kröger S, Richter JF, Wang J, Martin L, Bindelle J, et al. Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of pigs. J Nutr. 2012; 142:661-7. doi: 10.3945/jn.111.156190 PMID: 22357743
46. Smith AG, Reilly P, Sweeney T, Pierce KM, Gahan DA, Callan JJ, et al. The effect of cereal type and exogenous enzyme supplementation on intestinal microbiota and nutrient digestibility in finisher pigs. Livest Sci. 2010; 133:148-50.
47. Santacruz A, Collado MC, García-Valdés L, Segura MT, Martín-Lagos JA, Anjos T, et al. Gut microbiota composition is associated with body weight, weight gain and biochemical parameters in pregnant women. Br J Nutr. 2010; 104:83-92. doi: 10.1017/S0007114510000176 PMID: 20205964
48. Remely M, Dworzak S, Hippe B, Zwielehner J, Aumüller E, Brath H, et al. Abundance and diversity of microbiota in type 2 diabetes and obesity. J Diab Metab. 2013; 4:253.
49. Kailasapathy K. and Chin J. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol. 2000; 78:80-8. PMID: 10651933
50. Ramirez-Farias C, Slezak K, Fuller Z, Duncan A, Holtrop G, Louis P. Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Brit J Nutr. 2009; 101:541-50. doi: 10.1017/S0007114508019880 PMID: 18590586
51. Looft T, Allen HK, Cantarel BL, Levine UY, Bayles DO, Alt DP, et al. Bacteria, phages and pigs: the effects of in-feed antibiotics on the microbiome at different gut locations. ISME J. 2014; 8:1566-76. doi: 10.1038/ismej.2014.12 PMID: 24522263
52. Frese SA, Parker K, Calvert CC, Mills DA. Diet shapes the gut microbiome of pigs during nursing and weaning. Microbiome. 2015; 3:28. doi: 10.1186/s40168-015-0091-8 PMID: 26167280
53. Schwiertz A, Taras D, Schäfer K, Beijer S, Bos NA, Donus C, et al. Microbiota and SCFA in lean and overweight healthy subjects. Obesity. 2010; 18:190-5. doi: 10.1038/oby.2009.167 PMID: 19498350
54. Kalliomäki M, Collado MC, Salminen S, Isolauri E. Early differences in fecal microbiota composition in children may predict overweight. Am J Clin Nutr. 2008; 87:534-8. PMID: 18326589
55. Kim HB, Borewicz K, White BA, Singer RS, Sreevatsan S, Tu ZJ, et al. Longitudinal investigation of the age-related bacterial diversity in the feces of commercial pigs. Vet Microbiol. 2011; 153:124-33. doi: 10.1016/j.vetmic.2011.05.021 PMID: 21658864
56. Luoto R, Laitinen K, Nermes M, Isolauri E. Impact of maternal probiotic-supplemented dietary counselling on pregnancy outcome and prenatal and postnatal growth: a double-blind, placebo-controlled study. Br J Nutr. 2010; 103:1792-9. doi: 10.1017/S0007114509993898 PMID: 20128938
57. Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, et al. Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr. 2010; 64:636-43. doi: 10.1038/ejcn.2010.19 PMID: 20216555
58. 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. Int J Obes. 2013; 37:1460-6.
59. Drissi F, Merhej V, Angelakis E, El Kaoutari A, Carrière F, Henrissat B, et al. Comparative genomics analysis of Lactobacillus species associated with weight gain or weight protection. Nutr Diabetes.2014; 4:e109. doi: 10.1038/nutd.2014.6 PMID: 24567124
60. Topping DL, Clifton PM. Short-chain fatty acids and human colonic function: Roles of resistant starch and nonstarch polysaccharides. Physiol Rev. 2001; 81:1031-64. PMID: 11427691
61. den Besten G, van Eunen K, Groen AK, Venema K, Reijngoud DJ, Bakker BM. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 2013; 54:2325-40 doi: 10.1194/jlr.R036012 PMID: 23821742
62. Millet S, Van Oeckel MJ, Aluwé M, Delezie E, De Brabander DL. Prediction of in Vivo short-chain fatty acid production in hindgut fermenting mammals: Problems and pitfalls. Crit Rev Food Sci Nutr. 2010; 50:605-19. doi: 10.1080/10408390802565939 PMID: 20694924
63. Palmquist DL. The role of dietary fats in efficiency of ruminants. J Nutr. 1994; 124:1377S-1382S. PMID: 8064387
64. Zumbrun SD, Melton-Celsa AR, Smith MA, Gilbreath JJ, Merrell DS, O'Brien AD. Dietary choice affects Shiga toxin producing Escherichia coli (STEC) O157:H7 colonization and disease. Proc Natl Acad Sci USA. 2013; 110:2126-33.
65. Matise I, Sirinarumitr T, Bosworth BT, Moon HW. Vascular ultrastructure and DNA fragmentation in swine infected with Shiga toxin-producing Escherichia coli. Vet Pathol. 2000; 37:318-27. PMID: 10896393
66. Kaczmarczyk MM, Miller MJ, Freund GG. The health benefits of dietary fiber: Beyond the usual suspects of type 2 diabetes mellitus, cardiovascular disease and colon cancer. Metabolism. 2012; 61:1058-66. doi: 10.1016/j.metabol.2012.01.017 PMID: 22401879
67. Purushe J, Fouts DE, Morrison M, White BA, Mackie RI, Coutinho PM, et al. Comparative Genome Analysis of Prevotella ruminicola and Prevotella bryantii: insights into their environmental niche. Microbial Ecol. 2010; 60:721-29.
68. Pluske JR, Pethick DW, Hopwood DE, Hampson DJ. Nutritional influences on some major enteric bacterial diseases of pigs. Nutr Res Rev. 2002; 15:333-71. doi: 10.1079/NRR200242 PMID: 19087411
69. Wong JM, de Souza R, Kendall CW, Emam A, Jenkins DJ. Colonic health: fermentation and short chain fatty acids. J Clin Gastroenterol. 2006; 40:235-43. PMID: 16633129
70. Pang X, Hua X, Yang Q, Ding D, Che C, Cui L, et al. Inter-species transplantation of gut microbiota from human to pigs. ISME J. 2007; 1:156-62. PMID: 18043625
71. Shen J, Zhang B, Wei H, Che C, Ding D, Hua X, et al. Assessment of the modulating effects of fructooligosaccharides on fecal microbiota using human flora-associated piglets. Arch Microbiol. 2010; 192:959-68. doi: 10.1007/s00203-010-0628-y PMID: 20844866