Iron supplementation promotes gut microbiota metabolic activity but not colitis markers in human gut microbiota-associated rats

British Journal of Nutrition

Volumn 111, Issue 12, 2014, Pages 2135-2145

  Dostal, Alexandra ^a   Lacroix, Christophe ^a   Pham, Van T ^a   Zimmermann, Michael B ^a   Del'Homme, Christophe ^b   Bernalier Donadille, Annick ^b   Chassard, Christophe ^a  

^a ETH ZURICH   (Switzerland)

^b CEMAGREF   (France)

Author keywords

Butyrate; Colitis; Gut microbiota; Iron

Indexed keywords

IRON; RNA 16S;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTEROIDES; CECUM MICROFLORA; CLOSTRIDIUM; COLITIS; CONTROLLED STUDY; DIET SUPPLEMENTATION; ENTEROCOCCUS; FECES ANALYSIS; FECES MICROFLORA; FEMALE; HISTOLOGY; INTESTINE FLORA; IRON DEPLETION; IRON THERAPY; NONHUMAN; PYROSEQUENCING; RAT; TREATMENT DURATION; TREATMENT RESPONSE; WEIGHT GAIN;

BACTERIA (MICROORGANISMS); BACTEROIDES SP.; CLOSTRIDIUM; RATTUS;

ANIMALS; BACTEROIDES; BIOLOGICAL MARKERS; BUTYRIC ACID; CECUM; CHILD; CLOSTRIDIUM; COLITIS; COLON; DIETARY SUPPLEMENTS; DISEASE MODELS, ANIMAL; FECES; FEMALE; GERM-FREE LIFE; HUMANS; ILEUM; IMMUNITY, MUCOSAL; IRON; IRON, DIETARY; RATS; RATS, INBRED F344; WEIGHT GAIN;

EID: 84901341883     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S000711451400021X     Document Type: Article

References (78)

1. Guarner F (2006) Enteric flora in health and disease. Digestion 73, Suppl. 1, 5-12.
2. Sekirov I, Russell SL, Antunes LC, et al. (2010) Gut microbiota in health and disease. Physiol Rev 90, 859-904.
3. Kau AL, Ahern PP, Griffin NW, et al. (2011) Human nutrition, the gut microbiome and the immune system. Nature 474, 327-336.
4. Stecher B & Hardt WD (2011) Mechanisms controlling pathogen colonization of the gut. Curr Opin Microbiol 14, 82-91.
5. Louis P, McCrae SI, Charrier C, et al. (2007) Organization of butyrate synthetic genes in human colonic bacteria: phylogenetic conservation and horizontal gene transfer. FEMS Microbiol Lett 269, 240-247.
6. Hoyles L & Wallace RJ (2010) Gastrointestinal tract: intestinal fatty acid metabolism and implications for health. In Handbook of Hydrocarbon and Lipid Microbiology, pp. 3119-3132 [K Timmis, editor]. Berlin: Springer.
7. Scott KP, Gratz SW, Sheridan PO, et al. (2013) The influence of diet on the gut microbiota. Pharmacol Res 69, 52-60.
8. Louis P & Flint HJ (2009) Diversity, metabolism and microbial ecology of butyrate-producing bacteria from the human large intestine. FEMS Microbiol Lett 294, 1-8.
9. Pryde SE, Duncan SH, Hold GL, et al. (2002) The microbiology of butyrate formation in the human colon. FEMS Microbiol Lett 217, 133-139.
10. Roediger WE (1980) Role of anaerobic bacteria in the metabolic welfare of the colonic mucosa in man. Gut 21, 793-798.
11. Hamer HM, Jonkers D, Venema K, et al. (2008) Review Article: the role of butyrate on colonic function. Aliment Pharmacol Ther 27, 104-119.
12. Gantois I, Ducatelle R, Pasmans F, et al. (2006) Butyrate specifically down-regulates salmonella pathogenicity island 1 gene expression. Appl Environ Microbiol 72, 946-949.
13. FlintHJ,DuncanSH, ScottKP, etal. (2007) Interactions and competition within the microbial community of the human colon: links between diet and health. EnvironMicrobiol 9, 1101-1111.
14. De Vuyst L & Leroy F (2011) Cross-feeding between bifidobacteria and butyrate-producing colon bacteria explains bifidobacterial competitiveness, butyrate production, and gas production. Int J Food Microbiol 149, 73-80.
15. Gupta SS, Mohammed MH, Ghosh TS, et al. (2011) Metagenome of the gut of a malnourished child. Gut Pathog 3, 7.
16. Smith MI, Yatsunenko T, Manary MJ, et al. (2013) Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 339, 548-554.
17. Lin A, Bik EM, Costello EK, et al. (2013) Distinct distal gut microbiome diversity and composition in healthy children from Bangladesh and the United States. PLoS ONE 8, e53838.
18. Yatsunenko T, Rey FE, Manary MJ, et al. (2012) Human gut microbiome viewed across age and geography. Nature 486, 222-227.
19. Grzeskowiak L, Collado MC, Mangani C, et al. (2012) Distinct gut microbiota in southeastern African and northern European infants. J Pediatr Gastroenterol Nutr 54, 812-816.
20. De Filippo C, Cavalieri D, Di Paola M, et al. (2010) Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 107, 14691-14696.
21. Zimmermann MB & Hurrell RF (2007) Nutritional iron deficiency. Lancet 370, 511-520.
22. WHO (2002) Deficiency Anemia; Assessment, Prevention, and Control; A Guide for Programme Managers. Geneva: World Health Organization.
23. Lynch SR (2011) Why nutritional iron deficiency persists as a worldwide problem. J Nutr 141, 763S-768S.
24. Dostal A, Chassard C, Hilty FM, et al. (2012) Iron depletion and repletion with ferrous sulfate or electrolytic iron modifies the composition and metabolic activity of the gut microbiota in rats. J Nutr 142, 271-277.
25. Werner T, Wagner SJ, Martinez I, et al. (2011) Depletion of luminal iron alters the gut microbiota and prevents Crohn?s disease-like ileitis. Gut 60, 325-333.
26. Tompkins GR, O?Dell NL, Bryson IT, et al. (2001) The effects of dietary ferric iron and iron deprivation on the bacterial composition of the mouse intestine. Curr Microbiol 43, 38-42.
27. Dostal A, Fehlbaum S, Chassard C, et al. (2013) Low iron availability in continuous in vitro colonic fermentations induces strong dysbiosis of the child gut microbial consortium and a decrease in main metabolites. FEMS Microbiol Ecol 83, 161-175.
28. Hilty FM, Arnold M, Hilbe M, et al. (2010) Iron from nanocompounds containing iron and zinc is highly bioavailable in rats without tissue accumulation. Nat Nanotechnol 5, 374-380.
29. Lee SH, Shinde P, Choi J, et al. (2008) Effects of dietary iron levels on growth performance, hematological status, liver mineral concentration, fecal microflora, and diarrhea incidence in weanling pigs. Biol Trace Elem Res 126, Suppl. 1, S57-S68.
30. Zimmermann MB, Chassard C, Rohner F, et al. (2010) The effects of iron fortification on the gut microbiota in African children: a randomized controlled trial in Cote d?Ivoire. Am J Clin Nutr 92, 1406-1415.
31. Krebs NF, Sherlock LG, Westcott J, et al. (2013) Effects of different complementary feeding regimens on iron status and enteric microbiota in breastfed infants. J Pediatr 163, 416-423.
32. Buhnik-Rosenblau K, Moshe-Belizowski S, Danin-Poleg Y, et al. (2012) Genetic modification of iron metabolism in mice affects the gut microbiota. Biometals 25, 883-892.
33. Winter SE, Thiennimitr P, Winter MG, et al. (2010) Gut inflammation provides a respiratory electron acceptor for Salmonella. Nature 467, 426-429.
34. Winter SE, Lopez CA & Baumler AJ (2013) The dynamics of gut-associated microbial communities during inflammation. EMBO Rep 14, 319-327.
35. Dethlefsen L, McFall-Ngai M & Relman DA (2007) An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449, 811-818.
36. Alpert C, Sczesny S, Gruhl B, et al. (2008) Long-term stability of the human gut microbiota in two different rat strains. Curr Issues Mol Biol 10, 17-24.
37. Krych L, Hansen CH, Hansen AK, et al. (2013) Quantitatively different, yet qualitatively alike: a meta-analysis of the mouse core gut microbiome with a view towards the human gut microbiome. PLoS ONE 8, e62578.
38. Hanske L, Engst W, Loh G, et al. (2012) Contribution of gut bacteria to the metabolism of cyanidin 3-glucoside in human microbiota-associated rats. Br J Nutr 109, 1433-1441.
39. Wos-Oxley M, Bleich A, Oxley AP, et al. (2012) Comparative evaluation of establishing a human gut microbial community within rodent models. Gut Microbes 3, 234-249.
40. Crouzet L, Gaultier E, Del?homme C, et al. (2013) The hypersensitivity to colonic distension of IBS patients can be transferred to rats through their fecal microbiota. Neurogastroenterol Motil 25, e272-e282.
41. Iannotti LL, Tielsch JM, Black MM, et al. (2006) Iron supplementation in early childhood: health benefits and risks. Am J Clin Nutr 84, 1261-1276.
42. Forbes AL, Arnaud MJ, Chichester CO, et al. (1989) Comparison of in vitro, animal, and clinical determinations of iron bioavailability: International Nutritional Anemia Consultative Group Task Force report on iron bioavailability. Am J Clin Nutr 49, 225-238.
43. de Sablet T, Chassard C, Bernalier-Donadille A, et al. (2009) Human microbiota-secreted factors inhibit shiga toxin synthesis by enterohemorrhagic Escherichia coli O157:H7. Infect Immun 77, 783-790.
44. Reeves PG, Nielsen FH & Fahey GC Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123, 1939-1951.
45. Abatan OI, Welch KB & Nemzek JA (2008) Evaluation of saphenous venipuncture and modified tail-clip blood collection in mice. J Am Assoc Lab Anim Sci 47, 8-15.
46. Engel MA, Kellermann CA, Rau T, et al. (2008) Ulcerative colitis in AKR mice is attenuated by intraperitoneally administered anandamide. J Physiol Pharmacol 59, 673-689.
47. Zihler A, Gagnon M, Chassard C, et al. (2010) Unexpected consequences of administering bacteriocinogenic probiotic strains for Salmonella populations, revealed by an in vitro colonic model of the child gut. Microbiology 156, 3342-3353.
48. Pereyra LP, Hiibel SR, Prieto Riquelme MV, et al. (2010) Detection and quantification of functional genes of cellulose-degrading, fermentative, and sulfate-reducing bacteria and methanogenic archaea. Appl EnvironMicrobiol 76, 2192-2202.
49. Ramirez-Farias C, Slezak K, Fuller Z, et al. (2009) Effect of inulin on the human gut microbiota: stimulation of Bifidobacterium adolescentis and Faecalibacterium prausnitzii. Br J Nutr 101, 541-550.
50. Schloss PD, Westcott SL, Ryabin T, et al. (2009) Introducing mothur: open-source, platform-independent, communitysupported software for describing and comparing microbial communities. Appl Environ Microbiol 75, 7537-7541.
51. DeSantis TZ, Hugenholtz P, Larsen N, et al. (2006) Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 72, 5069-5072.
52. Edgar RC, Haas BJ, Clemente JC, et al. (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194-2200.
53. Cleusix V, Lacroix C, Vollenweider S, et al. (2008) Glycerol induces reuterin production and decreases Escherichia coli population in an in vitro model of colonic fermentation with immobilized human feces. FEMS Microbiol Ecol 63, 56-64.
54. Gootenberg DB & Turnbaugh PJ (2011) Companion animals symposium: humanized animal models of the microbiome. J Anim Sci 89, 1531-1537.
55. Kasaoka S, Yamagishi H & Kitano T (1999) Differences in the effect of iron-deficient diet on tissue weight, hemoglobin concentration and serum triglycerides in Fischer-344, Sprague-Dawley and Wistar rats. J Nutr Sci Vitaminol (Tokyo) 45, 359-366.
56. Lih-Brody L, Powell SR, Collier KP, et al. (1996) Increased oxidative stress and decreased antioxidant defenses in mucosa of inflammatory bowel disease. Dig Dis Sci 41, 2078-2086.
57. Seril DN, Liao J, Ho KL, et al. (2002) Dietary iron supplementation enhances DSS-induced colitis and associated colorectal carcinoma development in mice. Dig Dis Sci 47, 1266-1278.
58. Carrier JC, Aghdassi E, Jeejeebhoy K, et al. (2006) Exacerbation of dextran sulfate sodium-induced colitis by dietary iron supplementation: role of NF-kappaB. Int J Colorectal Dis 21, 381-387.
59. Perl DP, Fogarty U, Harpaz N, et al. (2004) Bacterial-metal interactions: the potential role of aluminum and other trace elements in the etiology of Crohn?s disease. Inflamm Bowel Dis 10, 881-883.
60. da Silva SM, Venceslau SS, Fernandes CL, et al. (2008) Hydrogen as an energy source for the human pathogen Bilophila wadsworthia. Antonie Van Leeuwenhoek 93, 381-390.
61. Calusinska M, Happe T, Joris B, et al. (2010) The surprising diversity of clostridial hydrogenases: a comparative genomic perspective. Microbiology 156, 1575-1588.
62. Balamurugan R, Mary RR, Chittaranjan S, et al. (2010) Low levels of faecal lactobacilli in women with iron-deficiency anaemia in south India. Br J Nutr 104, 931-934.
63. Cuiv PO, Klaassens ES, Durkin AS, et al. (2011) Draft genome sequence of Turicibacter sanguinis PC909, isolated from human feces. J Bacteriol 193, 1288-1289.
64. Arias CA & Murray BE (2012) The rise of the Enterococcus: beyond vancomycin resistance. Nat Rev Microbiol 10, 266-278.
65. Louis P, Young P, Holtrop G, et al. (2010) Diversity of human colonic butyrate-producing bacteria revealed by analysis of the butyryl-CoA:acetate CoA-transferase gene. Environ Microbiol 12, 304-314.
66. Karadag D & Puhakka JA (2010) Enhancement of anaerobic hydrogen production by iron and nickel. Int J Hydrogen Energy 35, 8554-8560.
67. Wei H, Dong L, Wang T, et al. (2010) Structural shifts of gut microbiota as surrogate endpoints for monitoring host health changes induced by carcinogen exposure. FEMS Microbiol Ecol 73, 577-586.
68. Conterno L, Fava F, Viola R, et al. (2011) Obesity and the gut microbiota: does up-regulating colonic fermentation protect against obesity and metabolic disease Genes Nutr 6, 241-260.
69. Hosseini E, Grootaert C, Verstraete W, et al. (2011) Propionate as a health-promoting microbial metabolite in the human gut. Nutr Rev 69, 245-258.
70. Luhrs H, Kudlich T, Neumann M, et al. (2002) Butyrateenhanced TNFalpha-induced apoptosis is associated with inhibition of NF-kappaB. Anticancer Res 22, 1561-1568.
71. Luhrs H, Gerke T, Muller JG, et al. (2002) Butyrate inhibits NF-kappaB activation in lamina propria macrophages of patients with ulcerative colitis. Scand J Gastroenterol 37, 458-466.
72. Roy MJ, Dionne S, Marx G, et al. (2009) In vitro studies on the inhibition of colon cancer by butyrate and carnitine. Nutrition 25, 1193-1201.
73. Chassard C, Dapoigny M, Scott KP, et al. (2012) Functional dysbiosis within the gut microbiota of patients with constipated-irritable bowel syndrome. Aliment Pharmacol Ther 35, 828-838.
74. Carbonero F, Benefiel AC, Alizadeh-Ghamsari AH, et al. (2012) Microbial pathways in colonic sulfur metabolism and links with health and disease. Front Physiol 3, 448.
75. Marquet P, Duncan SH, Chassard C, et al. (2009) Lactate has the potential to promote hydrogen sulphide formation in the human colon. FEMS Microbiol Lett 299, 128-134.
76. Attene-Ramos MS, Nava GM, Muellner MG, et al. (2010) DNA damage and toxicogenomic analyses of hydrogen sulfide in human intestinal epithelial FHs 74 Int cells. Environ Mol Mutagen 51, 304-314.
77. Wallace JL, Vong L, McKnight W, et al. (2009) Endogenous and exogenous hydrogen sulfide promotes resolution of colitis in rats. Gastroenterology 137, 569-578, 578 e561.
78. Hirata I, Naito Y, Takagi T, et al. (2011) Endogenous hydrogen sulfide is an anti-inflammatory molecule in dextran sodium sulfate-induced colitis in mice. Dig Dis Sci 56, 1379-1386.