Influence of whole-wheat consumption on fecal microbial community structure of obese diabetic mice

PeerJ

Volumn 2016, Issue 2, 2016, Pages

  Garcia Mazcorro, Jose F ^a   Ivanov, Ivan ^b   Mills, David A ^c   Noratto, Giuliana ^b,d  

^a UNIVERSIDAD AUTÓNOMA DE NUEVO LEÓN   (Mexico)

^b TEXAS A AND M UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d WASHINGTON STATE UNIVERSITY   (United States)

Author keywords

Fecal microbiota; High throughput sequencing; Metabolic pathways; Obesity; Whole wheat

Indexed keywords

SHORT CHAIN FATTY ACID; UNCLASSIFIED DRUG;

ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DIABETIC OBESITY; DIETARY COMPLIANCE; DNA EXTRACTION; FECES ANALYSIS; FECES MICROFLORA; GENE SEQUENCE; GENETIC ANALYSIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIGH THROUGHPUT SEQUENCING; INTESTINE FLORA; LACTOBACILLUS; METABOLISM; MOUSE; NONHUMAN; REAL TIME POLYMERASE CHAIN REACTION; RUMINOCOCCACEAE; WHEAT;

EID: 84963963443     PISSN: None     EISSN: 21678359     Source Type: Journal    
DOI: 10.7717/peerj.1702     Document Type: Article

References (52)

1. Bacchetti DG, Aldred N, Clare AS, Burgess JG. 2011. Improvement of phylumand class-specific primers for real-time PCR quantification of bacterial taxa. Journal of Microbiological Methods 86(3):351-356 DOI 10.1016/j.mimet.2011.06.010.
2. Bartosch S, Fite A, Macfarlane GT, McMurdo ME. 2004. Characterization of bacterial communities in feces from healthy elderly volunteers and hospitalized elderly patients by using real-time PCR and effects of antibiotic treatment on the fecal microbiota. Applied Environmental Microbiology 70(6):3575-3581 DOI 10.1128/AEM.70.6.3575-3581.2004.
3. Bermudez-Brito M, Sahasrabudhe NM, Rösch C, Schols HA, Faas MM, de Vos P. 2015. The impact of dietary fibers on dendritic cell responses in vitro is dependent on the differential effects of the fibers on intestinal epithelial cells. Molecular Nutrition and Food Research 30(4):698-710 DOI 10.1002/mnfr.201400811.
4. Bokulich NA, Thorngate JH, Richardson PM, Mills DA. 2014. Microbial biogeography of wine grapes is conditioned by cultivar, vintage, and climate. Proceedings of the National Academy of Sciences of the United States of America 111(1):E139-E148 DOI 10.1073/pnas.1317377110.
5. Campbell AM, Fleisher J, Sinigalliano C, White JR, Lopez JV. 2015. Dynamics of marine bacteria community diversity of the coastal waters of the reefs, inlets, and wastewater outfalls of southeast Florida. MicrobiologyOpen 4(3):390-408 DOI 10.1002/mbo3.245.
6. Campos D, Betalleluz-Pallardel I, Chirinos R, Aguilar-Galvez A, Noratto G, Pedreschi R. 2012. Prebiotic effects of yacon (Smallanthus sonchifolius Poepp. & Endl), a source of fructooligosaccharides and phenolic compounds with antioxidant activity. Food Chemistry 135(3):1592-1599 DOI 10.1016/j.foodchem.2012.05.088.
7. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koening JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turbnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R. 2010. QIIME allows analysis of high-throughput community sequencing data. Nature Methods 7:335-336 DOI 10.1038/nmeth.f.303.
8. Cheng KK, Wang GY, Zeng J, Zhang JA. 2013. Improved succinate production by metabolic engineering. BioMed Research International 2013:538790 DOI 10.1155/2013/538790.
9. Collado MC, Derrien M, Isolauri E, de Vos WM, Saliminen S. 2007. Intestinal integrity and Akkermansia muciniphila, a mucin-degrading member of the intestinal microbiota present in infants, adults, and the elderly. Applied Environmental Microbiology 73(23):7767-7770 DOI 10.1128/AEM.01477-07.
10. Delzenne NM, Cani PD. 2011. Interaction between obesity and the gut microbiota: relevance in nutrition. Annual Review of Nutrition 31:15-31 DOI 10.1146/annurev-nutr-072610-145146.
11. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL. 2006. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Applied Environmental Microbiology 72(7):5069-5072 DOI 10.1128/AEM.03006-05.
12. Donohoe DR, Garge N, Zhang X, Sun W, O'Connell TM, Bunger MK, Bultman SJ. 2013. The microbiome and butyrate regulate energy metabolism and autophagy in the mammalian colon. Cell Metabolism 13(5):517-526 DOI 10.1016/j.cmet.2011.02.018.
13. Duncan SH, Lobley GE, Holtrop G, Ince J, Johnstone AM, Louis P, Flint HJ. 2008. Human colonic microbiota associated with diet, obesity and weight loss. International Journal of Obesity 32:1720-1724 DOI 10.1038/ijo.2008.155.
14. Edgar RC. 2010. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26(19):2460-2461 DOI 10.1093/bioinformatics/btq461.
15. Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM. 2013. Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. Proceedings of the National Academy of Sciences of the United States of America 110(22):9066-9071 DOI 10.1073/pnas.1219451110.
16. Fernandes J, Su W, Rahat-Rozenbloom S, Wolever TM, Comelli EM. 2014. Adiposity, gut microbiota and faecal short chain fatty acids are linked in adult humans. Nutrition & Diabetes 4:e121 DOI 10.1038/nutd.2014.23.
17. Garcia-Mazcorro JF, Suchodolski JS, Jones KR, Clark-Price SC, Dowd SE, Minamoto Y, Markel M, Steiner JM, Dossin O. 2012. Effect of the proton pump inhibitor omeprazole on the gastrointestinal bacterial microbiota of healthy dogs. FEMS Microbiology Ecology 80(3):624-636 DOI 10.1111/j.1574-6941.2012.01331.x.
18. Guo X, Xia X, Tang R, Zhou J, Zhao H, Wang K. 2008. 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. Letters in Applied Microbiology 47(5):367-373 DOI 10.1111/j.1472-765X.2008.02408.x.
19. Gupta H. 2014. Barriers to and facilitators of long term weight loss maintenance in adult UK people: a thematic analysis. International Journal of Preventive Medicine 5(12):1512-1520.
20. Hammer Ø, Harper DAT, Ryan PD. 2001. PAST: paleontological statistics software package for education and data analysis. Paleontologia Electronica 4:1-9.
21. Huijsdens XW, Linskens RK, Mak M, Meuwissen SGM, Vandenbroucke-Grauls CMJE, Savelkoul PHM. 2002. Quantification of bacteria adherent to gastrointestinal mucosa by real-time PCR. Journal of Clinical Microbiology 40(12):4423-4427 DOI 10.1128/JCM.40.12.4423-4427.2002.
22. Igarashi H, Maeda S, Ohno K, Horigome A, Odamaki T, Tsujimoto H. 2014. Effect of oral administration of metronidazole or prednisolone on fecal microbiota in dogs. PLoS ONE 9(9):e107909 DOI 10.1371/journal.pone.0107909.
23. Jakobsdottir G, Xu J, Molin G, Ahrné S, Nyman M. 2013. High-fat diet reduces the formation of butyrate, but increases succinate, inflammation, live fat and cholesterol in rats, while dietary fibre counteracts these effects. PLoS ONE 8(11):e80476 DOI 10.1371/journal.pone.0080476.
24. Kanehisa M, Goto S, Sato Y, Furumichi M, Tanabe M. 2012. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research 40(D1):D109-D114 DOI 10.1093/nar/gkr988.
25. Katcher HI, Legro RS, Kunselman AR, Gillies PJ, Demers LM, Bagshaw DM, Kris-Etherton PM. 2008. The effects of a whole grain-enriched hypocaloric diet on cardiovascular disease risk factors in men and women with metabolic syndrome. The American Journal of Clinical Nutrition 87(1):79-90.
26. Kristensen M, Toubro S, Jensen MG, Ross AB, Riboldi G, Petronio M, Bügel S, Tetens I, Astrup A. 2011.Whole grain compared with refined wheat decreases the percentage of body fat following a 12-week, energy-restricted dietary intervention in postmenopausal women. Journal of Nutrition 142(4):710-716 DOI 10.3945/jn.111.142315.
27. Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C. 2013. Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology 31:814-823 DOI 10.1038/nbt.2676.
28. Larsen N, Vogensen FK, van den Berg FW, Nielsen DS, Andreasen AS, Pedersen BK, Al-Soud WA, Sørensen SJ, Hansen LH, Jakobsen M. 2010. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE 5(2):e9085 DOI 10.1371/journal.pone.0009085.
29. Ley RE, Bäckhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI. 2005. Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America 102(31):11070-11075 DOI 10.1073/pnas.0504978102.
30. Liu C, Song Y, McTeague M, Vu AW, Wexler H, Finegold SM. 2003. Rapid identification of the species of the Bacteroides fragilis group by multiplex PCR assays using groupand species-specific primers. FEMS Microbiology Letters 222(1):9-16 DOI 10.1016/S0378-1097(03)00296-9.
31. Louis P, Flint HJ. 2009. Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiology Letters 294(1):1-8 DOI 10.1111/j.1574-6968.2009.01514.x.
32. Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R. 2012. Diversity, stability and resilience of the human gut microbiota. Nature 489:220-230 DOI 10.1038/nature11550.
33. Lozupone CA, Hamady M, Kelley ST, Knight R. 2007. Quantitative and qualitative beta diversity measures lead to different insights into factors that structure microbial communities. Applied Environmental Microbiology 73(5):1576-1585 DOI 10.1128/AEM.01996-06.
34. Markowitz VM, Chen IM, Palaniappan K, Chu K, Szeto E, Grechkin Y, Ratner A, Jacob B, Huang J, Williams P, Huntemann M, Anderson I, Mavromatis K, Ivanova NN, Kyrpides NC. 2012. IMG: the Integrated Microbial Genomes database and comparative analysis system. Nucleic Acids Research 40(D1):D115-D122 DOI 10.1093/nar/gkr1044.
35. Neyrinck AM, Possemiers S, Druart C, van de Wiele T, De Backer F, Cani PD, Larondelle Y, Delzenne NM. 2011. Prebiotic effects of wheat arabinoxylan related to the increase in bifidobacteria, roseburia and bacteroides/prevotella in diet-induced obese mice. PLoS ONE 6(6):e20944 DOI 10.1371/journal.pone.0020944.
36. Noratto G, Garcia-Mazcorro JF, Markel M, Martino HS, Minamoto Y, Steiner JM, Byrne D, Suchodolski JS, Mertens-Talcott SU. 2014. Carbohydrate-free peach and plum juice affects fecal microbial ecology in an obese animal model. PLoS ONE 9(7):e101723 DOI 10.1371/journal.pone.0101723.
37. Oishi K, Yamamoto S, Itoh N, Nakao R, Yasumoto Y, Tanaka K, Kikuchi Y, Fukudome S, Okita K, Takano-Ishikawa Y. 2015. Wheat alkylresorcinols suppress high-fat, high-sucrose diet-induced obesity and glucose intolerance by increasing insulin sensitivity and cholesterol excretion in male mice. Journal of Nutrition 145(2):199-206 DOI 10.3945/jn.114.202754.
38. Parks DH, Beiko RG. 2010. Identifying biologically relevant differences between metagenomic communities. Bioinformatics 26(6):715-721 DOI 10.1093/bioinformatics/btq041.
39. Penders J, Vink C, Driessen C, London N, Thijs C, Stobberingh EE. 2005. Quantificacion of Bifidobacterium spp., Escherichia coli and Clostridium difficile in faecal samples of breastfed and formula-fed infants by real-time PCR. FEMS Microbiology Letters 243(1):141-147.
40. Petschow B, Doré J, Hibberd P, Dinan T, Reid G, Blaser M, Cani PD, Degnan FH, Foster J, Gibson G, Hutton J, Klaenhammer TR, Ley R, Nieuwdorp M, Pot B, Relman D, Serazin A, Sanders ME. 2013. Probiotics, prebiotics, and the host microbiome: the science of translation. Annals of the New York Academy of Sciences 1306:1-17 DOI 10.1111/nyas.12303.
41. R Core Team. 2014. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at http://www. R-project.org/.
42. Reichardt N, Duncan SH, Young P, Belenguer A, Leitch CM, Scott KP, Flint HJ, Louis P. 2014. Phylogenetic distribution of three pathways for propionate production within the human gut microbiota. ISME Journal 8:1323-1335 DOI 10.1038/ismej.2014.14.
43. Rideout JR, He Y, Navas-Molina JA, WaltersWA, Ursell LK, Gibbons SM, Chase J, McDonald D, Gonzalez A, Robbins-Pianka A, Clemente JC, Gilbert JA, Huse SM, Zhou HW, Knight R, Caporaso JG. 2014. Subsampled open-reference clustering creates consistent, comprehensive OTU definitions and scales to billions of sequences. PeerJ 2:e545 DOI 10.7717/peerj.545.
44. Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB, Lesniewski RA, Oakley BB, Parks DH, Robinson CJ, Sahl JW, Stres B, Thallinger GG, Van Horn DJ, Weber CF. 2009. Introducing mothur: open source, platform-independent, communitysupported software for describing and comparing microbial communities. Applied Environmental Microbiology 75(23):7537-7541 DOI 10.1128/AEM.01541-09.
45. Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C. 2011. Metagenomic biomarker discovery and explanation. Genome Biology 12:R60 DOI 10.1186/gb-2011-12-6-r60.
46. Stevenson L, Phillips F, O'Sullivan K, Walton J. 2012. Wheat bran: its composition and benefits to health, a European perspective. International Journal of Food Sciences and Nutrition 63(8):1001-1013 DOI 10.3109/09637486.2012.687366.
47. Suchodolski JS, Markel ME, Garcia-Mazcorro JF, Unterer S, Heilmann RM, Dowd SE, Kachroo P, Ivanov I, Minamoto Y, Dillman EM, Steiner JM, Cook AK, Toresson L. 2012. The fecal microbiome in dogs with acute diarrhea and idiopathic inflammatory bowel disease. PLoS ONE 7(12):e51907 DOI 10.1371/journal.pone.0051907.
48. Turnbaugh PJ, Bäckhed F, Fulton L, Gordon JI. 2008. Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome. Cell Host & Microbe 17(4):213-223 DOI 10.1016/j.chom.2008.02.015.
49. Vitaglione P, Mennella I, Ferracane R, Rivellese AA, Giacco R, Ercolini D, Gibbons SM, La Storia A, Gilbert JA, Jonnalagadda S, Thielecke F, Gallo MA, ScalfiL, Fogliano V. 2015. Whole-grain wheat consumption reduces inflammation in a randomized controlled trial on overweight and obese subjects with unhealthy dietary and lifestyle behaviors: role of polyphenolics bounds to cereal dietary fiber. American Journal of Clinical Nutrition 101(2):251-261 DOI 10.3945/ajcn.114.088120.
50. Walter J, Tannock GW, Tilsala-Timisjarvi A, Rodtong S, Loach DM, Munro K, Alatossava T. 2000. Detection and identification of gastrointestinal Lactobacillus species by using denaturing gel electrophoresis and species-specific PCR primers. Applied Environmental Microbiology 66(1):297-303.
51. Wu GD, Lewis JD, Hoffmann C, Chen YY, Knight R, Bittinger K, Hwang J, Chen J, Berkowsky R, Nessel L, Li H, Bushman FD. 2010. Sampling and pyrosequencing methods for characterizing bacterial communities in the human gut using 16S sequence tags. BMC Microbiology 10:206 DOI 10.1186/1471-2180-10-206.
52. Zhang H, DiBaise JK, Zuccolo A, Kudrna D, Braidotti M, Yu Y, Parameswaran P, Crowell MD, Wing R, Rittmann BE, Krajmalnik-Brown R. 2009. Human gut microbiota in obesity and after gastric bypass. Proceedings of the National Academy of Sciences of the United States of America 106(7):2365-2370 DOI 10.1073/pnas.0812600106.