Lactulose Differently Modulates the Composition of Luminal and Mucosal Microbiota in C57BL/6J Mice

Journal of Agricultural and Food Chemistry

Volumn 64, Issue 31, 2016, Pages 6240-6247

  Mao, Bingyong ^a   Li, Dongyao ^a   Ai, Chunqing ^b   Zhao, Jianxin ^a   Zhang, Hao ^a   Chen, Wei ^a,c  

^a JIANGNAN UNIVERSITY   (China)

^b DALIAN POLYTECHNIC UNIVERSITY   (China)

^c BEIJING TECHNOLOGY AND BUSINESS UNIVERSITY   (China)

Author keywords

Bifidobacterium; Helicobacter; lactulose; luminal; mucosal

Indexed keywords

FATTY ACIDS; MAMMALS;

BIFIDOBACTERIUM; HELICOBACTER; LACTULOSE; LUMINAL; MUCOSAL;

BODY FLUIDS;

LACTULOSE; VOLATILE FATTY ACID;

ANIMAL; BACTERIUM; C57BL MOUSE; CECUM; CLASSIFICATION; COLON; INTESTINE FLORA; INTESTINE MUCOSA; ISOLATION AND PURIFICATION; METABOLISM; MICROBIOLOGY; MOUSE;

ANIMALS; BACTERIA; CECUM; COLON; FATTY ACIDS, VOLATILE; GASTROINTESTINAL MICROBIOME; INTESTINAL MUCOSA; LACTULOSE; MICE; MICE, INBRED C57BL;

EID: 84981713426     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/acs.jafc.6b02305     Document Type: Article

References (44)

1. Eckburg, P. B.; Bik, E. M.; Bernstein, C. N.; Purdom, E.; Dethlefsen, L.; Sargent, M.; Gill, S. R.; Nelson, K. E.; Relman, D. A. Diversity of the human intestinal microbial flora Science 2005, 308, 1635-1638 10.1126/science.1110591
2. Cani, P. D.; Bibiloni, R.; Knauf, C.; Waget, A.; Neyrinck, A. M.; Delzenne, N. M.; Burcelin, R. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice Diabetes 2008, 57, 1470-1481 10.2337/db07-1403
3. Greenblum, S.; Turnbaugh, P. J.; Borenstein, E. Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 594-599 10.1073/pnas.1116053109
4. Benson, A. K.; Kelly, S. A.; Legge, R.; Ma, F. R.; Low, S. J.; Kim, J.; Zhang, M.; Oh, P. L.; Nehrenberg, D.; Hua, K. J.; Kachman, S. D.; Moriyama, E. N.; Walter, J.; Peterson, D. A.; Pomp, D. Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 18933-18938 10.1073/pnas.1007028107
5. Carmody, R. N.; Gerber, G. K.; Luevano, J. M.; Gatti, D. M.; Somes, L.; Svenson, K. L.; Turnbaugh, P. J. Diet dominates host genotype in shaping the murine gut microbiota Cell Host Microbe 2015, 17, 72-84 10.1016/j.chom.2014.11.010
6. Muegge, B. D.; Kuczynski, J.; Knights, D.; Clemente, J. C.; Gonzalez, A.; Fontana, L.; Henrissat, B.; Knight, R.; Gordon, J. I. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans Science 2011, 332, 970-974 10.1126/science.1198719
7. De Filippo, C.; Cavalieri, D.; Di Paola, M.; Ramazzotti, M.; Poullet, J. B.; Massart, S.; Collini, S.; Pieraccini, G.; Lionetti, P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa Proc. Natl. Acad. Sci. U. S. A. 2010, 107, 14691-14696 10.1073/pnas.1005963107
8. Claesson, M. J.; Jeffery, I. B.; Conde, S.; Power, S. E.; O'Connor, E. M.; Cusack, S.; Harris, H. M. B.; Coakley, M.; Lakshminarayanan, B.; O'Sullivan, O.; Fitzgerald, G. F.; Deane, J.; O'Connor, M.; Harnedy, N.; O'Connor, K.; O'Mahony, D.; van Sinderen, D.; Wallace, M.; Brennan, L.; Stanton, C.; Marchesi, J. R.; Fitzgerald, A. P.; Shanahan, F.; Hill, C.; Ross, R. P.; O'Toole, P. W. Gut microbiota composition correlates with diet and health in the elderly Nature 2012, 488, 178-184 10.1038/nature11319
9. Halmos, E. P.; Christophersen, C. T.; Bird, A. R.; Shepherd, S. J.; Gibson, P. R.; Muir, J. G. Diets that differ in their FODMAP content alter the colonic luminal microenvironment Gut 2015, 64, 93-100 10.1136/gutjnl-2014-307264
10. Marteau, P.; Pochart, P.; Dore, J.; Bera-Maillet, C.; Bernalier, A.; Corthier, G. Comparative study of bacterial groups within the human cecal and fecal microbiota Appl. Environ. Microbiol. 2001, 67, 4939-4942 10.1128/AEM.67.10.4939-4942.2001
11. Van den Abbeele, P.; Gerard, P.; Rabot, S.; Bruneau, A.; El Aidy, S.; Derrien, M.; Kleerebezem, M.; Zoetendal, E. G.; Smidt, H.; Verstraete, W.; Van de Wiele, T.; Possemiers, S. Arabinoxylans and inulin differentially modulate the mucosal and luminal gut microbiota and mucin-degradation in humanized rats Environ. Microbiol. 2011, 13, 2667-2680 10.1111/j.1462-2920.2011.02533.x
12. Johansson, M. E. V.; Larsson, J. M. H.; Hansson, G. C. The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions Proc. Natl. Acad. Sci. U. S. A. 2011, 108, 4659-4665 10.1073/pnas.1006451107
13. Derrien, M.; van Passel, M. W.; van de Bovenkamp, J. H.; Schipper, R. G.; de Vos, W. M.; Dekker, J. Mucin-bacterial interactions in the human oral cavity and digestive tract Gut Microbes 2010, 1, 254-268 10.4161/gmic.1.4.12778
14. Petuely, F. Lactobacillus bifidus flora produced in artificially-fed infants by bifidogenic substances (bifidus factor) Eur. J. Pediatr. 1957, 79, 174-179 10.1007/BF00440162
15. Panesar, P. S.; Kumari, S. Lactulose: Production, purification and potential applications Biotechnol. Adv. 2011, 29, 940-948 10.1016/j.biotechadv.2011.08.008
16. Tuohy, K. M.; Ziemer, C. J.; Klinder, A.; Knobel, Y.; Pool-Zobel, B. L.; Gibson, G. R. A human volunteer study to determine the prebiotic effects of lactulose powder on human colonic microbiota Microb. Ecol. Health Dis. 2002, 14, 165-173 10.1080/089106002320644357
17. Venema, K.; van Nuenen, M. H. M. C.; Van den Heuvel, E. G.; Pool, W.; van der Vossen, J. M. B. M. The effect of lactulose on the composition of the intestinal microbiota and short-chain fatty acid production in human volunteers and a computer-controlled model of the proximal large intestine Microb. Ecol. Health Dis. 2003, 15, 94-105 10.1080/08910600310019895
18. Vanhoutte, T.; De Preter, V.; De Brandt, E.; Verbeke, K.; Swings, J.; Huys, G. Molecular monitoring of the fecal microbiota of healthy human subjects during administration of lactulose and Saccharomyces boulardii Appl. Environ. Microbiol. 2006, 72, 5990-5997 10.1128/AEM.00233-06
19. Mao, B.; Li, D.; Zhao, J.; Liu, X.; Gu, Z.; Chen, Y. Q.; Zhang, H.; Chen, W. Metagenomic insights into the effects of fructo-oligosaccharides (FOS) on the composition of fecal microbiota in mice J. Agric. Food Chem. 2015, 63, 856-863 10.1021/jf505156h
20. Gu, S. H.; Chen, D. D.; Zhang, J. N.; Lv, X. M.; Wang, K.; Duan, L. P.; Nie, Y.; Wu, X. L. Bacterial community mapping of the mouse gastrointestinal tract PLoS One 2013, 8, e74957 10.1371/journal.pone.0074957
21. Campbell, J. M.; Fahey, G. C.; Wolf, B. W. Selected indigestible oligosaccharides affect large bowel mass, cecal and fecal short-chain fatty acids, pH and microflora in rats J. Nutr. 1997, 127, 130-136
22. Gustafsson, J. K.; Ermund, A.; Johansson, M. E.; Schutte, A.; Hansson, G. C.; Sjovall, H. An ex vivo method for studying mucus formation, properties, and thickness in human colonic biopsies and mouse small and large intestinal explants Am. J. Physiol.- Gastr. L. 2012, 302, G430-438 10.1152/ajpgi.00405.2011
23. Dotz, V.; Rudloff, S.; Meyer, C.; Lochnit, G.; Kunz, C. Metabolic fate of neutral human milk oligosaccharides in exclusively breastfed infants Mol. Nutr. Food Res. 2015, 59, 355-364 10.1002/mnfr.201400160
24. Zhang, Z.; Wang, H.; Yang, R.; Jiang, X. A novel spectrophotometric method for quantitative determination of lactulose in food industries Int. J. Food Sci. Technol. 2010, 45, 258-264 10.1111/j.1365-2621.2009.02129.x
25. Chaney, A. L.; Marbach, E. P. Modified reagents for determination of urea and ammonia Clin. Chem. 1962, 8, 130-132
26. Zhao, L. L.; Wang, G.; Siegel, P.; He, C.; Wang, H. Z.; Zhao, W. J.; Zhai, Z. X.; Tian, F. W.; Zhao, J. X.; Zhang, H.; Sun, Z. K.; Chen, W.; Zhang, Y.; Meng, H. Quantitative genetic background of the host influences gut microbiomes in chickens Sci. Rep. 2013, 3, 1163 10.1038/srep01163
27. Wang, Q.; Garrity, G. M.; Tiedje, J. M.; Cole, J. R. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy Appl. Environ. Microbiol. 2007, 73, 5261-5267 10.1128/AEM.00062-07
28. Caporaso, J. G.; Bittinger, K.; Bushman, F. D.; DeSantis, T. Z.; Andersen, G. L.; Knight, R. PyNAST: a flexible tool for aligning sequences to a template alignment Bioinformatics 2010, 26, 266-267 10.1093/bioinformatics/btp636
29. Caporaso, J. G.; Kuczynski, J.; Stombaugh, J.; Bittinger, K.; Bushman, F. D.; Costello, E. K.; Fierer, N.; Pena, A. G.; Goodrich, J. K.; Gordon, J. I.; Huttley, G. A.; Kelley, S. T.; Knights, D.; Koenig, J. E.; Ley, R. E.; Lozupone, C. A.; McDonald, D.; Muegge, B. D.; Pirrung, M.; Reeder, J.; Sevinsky, J. R.; Turnbaugh, P. J.; Walters, W. A.; Widmann, J.; Yatsunenko, T.; Zaneveld, J.; Knight, R. QIIME allows analysis of high-throughput community sequencing data Nat. Methods 2010, 7, 335-336 10.1038/nmeth.f.303
30. Price, M. N.; Dehal, P. S.; Arkin, A. P. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix Mol. Biol. Evol. 2009, 26, 1641-1650 10.1093/molbev/msp077
31. Lozupone, C.; Knight, R. UniFrac: a new phylogenetic method for comparing microbial communities Appl. Environ. Microbiol. 2005, 71, 8228-8235 10.1128/AEM.71.12.8228-8235.2005
32. Mao, B.; Li, D.; Zhao, J.; Liu, X.; Gu, Z.; Chen, Y. Q.; Zhang, H.; Chen, W. In vitro fermentation of lactulose by human gut bacteria J. Agric. Food Chem. 2014, 62, 10970-10977 10.1021/jf503484d
33. Bown, R. L.; Gibson, J. A.; Sladen, G. E.; Hicks, B.; Dawson, A. M. Effects of lactulose and other laxatives on ileal and colonic pH as measured by a radiotelemetry device Gut 1974, 15, 999-1004 10.1136/gut.15.12.999
34. McNeil, N. I.; Cummings, J. H.; James, W. P. T. Short chain fatty acid absorption by the human large intestine Gut 1978, 19, 819-822 10.1136/gut.19.9.819
35. Giller, J.; Phillips, S. F. Electrolyte absorption and secretion in the human colon Am. J. Dig. Dis. 1972, 17, 1003-1011 10.1007/BF02239140
36. Vince, A. J.; Burridge, S. M. Ammonia production by intestinal bacteria: the effects of lactose, lactulose and glucose J. Med. Microbiol. 1980, 13, 177-191 10.1099/00222615-13-2-177
37. Gill, H. S.; Guarner, F. Probiotics and human health: a clinical perspective Postgrad. Med. J. 2004, 80, 516-526 10.1136/pgmj.2003.008664
38. Picard, C.; Fioramonti, J.; Francois, J.; Robinson, T.; Neant, F.; Matuchansky, C. Review article: bifidobacteria as probiotic agents-physiological effects and clinical benefits Aliment. Pharmacol. Ther. 2005, 22, 495-512 10.1111/j.1365-2036.2005.02615.x
39. Derrien, M.; Vaughan, E. E.; Plugge, C. M.; de Vos, W. M. Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium Int. J. Syst. Evol. Microbiol. 2004, 54, 1469-1476 10.1099/ijs.0.02873-0
40. Barcelo, A.; Claustre, J.; Moro, F.; Chayvialle, J. A.; Cuber, J. C.; Plaisancie, P. Mucin secretion is modulated by luminal factors in the isolated vascularly perfused rat colon Gut 2000, 46, 218-224 10.1136/gut.46.2.218
41. Shimotoyodome, A.; Meguro, S.; Hase, T.; Tokimitsu, I.; Sakata, T. Short chain fatty acids but not lactate or succinate stimulate mucus release in the rat colon Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol. 2000, 125, 525-531 10.1016/S1095-6433(00)00183-5
42. Zhang, L.; Day, A.; McKenzie, G.; Mitchell, H. Nongastric Helicobacter species detected in the intestinal tract of children J. Clin. Microbiol. 2006, 44, 2276-2279 10.1128/JCM.02017-05
43. Fox, J. G. The non-H. pylori helicobacters: their expanding role in gastrointestinal and systemic diseases Gut 2002, 50, 273-283 10.1136/gut.50.2.273
44. Ruas-Madiedo, P.; Gueimonde, M.; Fernandez-Garcia, M.; de los Reyes-Gavilan, C. G.; Margolles, A. Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota Appl. Environ. Microbiol. 2008, 74, 1936-1940 10.1128/AEM.02509-07