The gastrointestinal microbiome: A malleable, third genome of mammals

Mammalian Genome

Volumn 20, Issue 7, 2009, Pages 395-403

  Carroll, Ian M ^a   Threadgill, David W ^a,b   Threadgill, Deborah S ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b NORTH CAROLINA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLACEBO; PREBIOTIC AGENT; PROBIOTIC AGENT;

CLINICAL TRIAL; COLITIS; COLON CANCER; CROHN DISEASE; DRUG EFFICACY; ECOSYSTEM; ENTERITIS; GASTROINTESTINAL TRACT; GENOME; HEALTH STATUS; HUMAN; INTESTINE FLORA; IRRITABLE COLON; LACTOBACILLUS DELBRUECKII; LACTOBACILLUS GASSERI; MAMMAL; MICROBIOME; MITOCHONDRIAL GENOME; NONHUMAN; OBESITY; REVIEW; ULCERATIVE COLITIS;

ANIMALS; BACTERIA; BACTERIAL INFECTIONS; GASTROINTESTINAL TRACT; GENOME, BACTERIAL; HUMANS; MAMMALS; METAGENOME;

MAMMALIA;

EID: 69249210949     PISSN: 09388990     EISSN: 14321777     Source Type: Journal    
DOI: 10.1007/s00335-009-9204-7     Document Type: Review

References (97)

1. DA Alexander RP Orcutt JC Henry J Baker Jr AC Bissahoyo, et al. 2006 Quantitative PCR assays for mouse enteric flora reveal strain-dependent differences in composition that are influenced by the microenvironment Mamm Genome 17 1093 1104
2. E Altermann WM Russell MA Azcarate-Peril R Barrangou BL Buck, et al. 2005 Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM Proc Natl Acad Sci USA 102 3906 3912
3. F Backhed RE Ley JL Sonnenburg DA Peterson JI Gordon 2005 Host-bacterial mutualism in the human intestine Science 307 1915 1920
4. F Backhed JK Manchester CF Semenkovich JI Gordon 2007 Mechanisms underlying the resistance to diet-induced obesity in germ-free mice Proc Natl Acad Sci USA 104 979 984
5. R Balamurugan E Rajendiran S George GV Samuel BS Ramakrishna 2008 Real-time polymerase chain reaction quantification of specific butyrate-producing bacteria, Desulfovibrio and Enterococcus faecalis, in the feces of patients with colorectal cancer J Gastroenterol Hepatol 23 1298 1303
6. E Bauer BA Williams H Smidt MW Verstegen R Mosenthin 2006 Influence of the gastrointestinal microbiota on development of the immune system in young animals Curr Issues Intest Microbiol 7 35 51
7. A Belenguer SH Duncan AG Calder G Holtrop P Louis, et al. 2006 Two routes of metabolic cross-feeding between Bifidobacterium adolescentis and butyrate-producing anaerobes from the human gut Appl Environ Microbiol 72 3593 3599
8. MF Bernet-Camard V Lievin D Brassart JR Neeser AL Servin, et al. 1997 The human Lactobacillus acidophilus strain LA1 secretes a nonbacteriocin antibacterial substance(s) active in vitro and in vivo Appl Environ Microbiol 63 2747 2753
9. R Bibiloni RN Fedorak GW Tannock KL Madsen P Gionchetti, et al. 2005 VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis Am J Gastroenterol 100 1539 1546
10. R Bibiloni M Mangold KL Madsen RN Fedorak GW Tannock 2006 The bacteriology of biopsies differs between newly diagnosed, untreated Crohn's disease and ulcerative colitis patients J Med Microbiol 55 1141 1149
11. JM Brulc DA Antonopoulos ME Miller MK Wilson AC Yannarell, et al. 2009 Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage-specific glycoside hydrolases Proc Natl Acad Sci USA 106 1948 1953
12. RC Brunham FA Plummer RS Stephens 1993 Bacterial antigenic variation, host immune response, and pathogen-host coevolution Infect Immun 61 2273 2276
13. IM Carroll JM Andrus JM Bruno-Barcena TR Klaenhammer HM Hassan, et al. 2007 Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse models of colitis Am J Physiol Gastrointest Liver Physiol 293 G729 G738
14. TL Chang CH Chang DA Simpson Q Xu PK Martin, et al. 2003 Inhibition of HIV infectivity by a natural human isolate of Lactobacillus jensenii engineered to express functional two-domain CD4 Proc Natl Acad Sci USA 100 11672 11677
15. SP Claus TM Tsang Y Wang O Cloarec E Skordi, et al. 2008 Systemic multicompartmental effects of the gut microbiome on mouse metabolic phenotypes Mol Syst Biol 4 219
16. Crawford PA, Crowley JR, Sambandam N, Muegge BD, Costello EK et al (2009) Regulation of myocardial ketone body metabolism by the gut microbiota during nutrient deprivation. Proc Natl Acad Sci USA [Epub ahead of print]
17. L Dethlefsen M McFall-Ngai DA Relman 2007 An ecological and evolutionary perspective on human-microbe mutualism and disease Nature 449 811 818
18. WF Dove L Clipson KA Gould C Luongo DJ Marshall, et al. 1997 Intestinal neoplasia in the ApcMin mouse: independence from the microbial and natural killer (beige locus) status Cancer Res 57 812 814
19. S Drouault C Juste P Marteau P Renault G Corthier 2002 Oral treatment with Lactococcus lactis expressing Staphylococcus hyicus lipase enhances lipid digestion in pigs with induced pancreatic insufficiency Appl Environ Microbiol 68 3166 3168
20. ME Dumas RH Barton A Tove O Cloarec C Blancher, et al. 2006 Metabolic profiling reveals a contribution of gut microbiota to fatty liver phenotype in insulin-resistant mice Proc Natl Acad Sci USA 103 12511 12516
21. SH Duncan A Belenguer G Holtrop AM Johnstone HJ Flint, et al. 2007 Reduced dietary intake of carbohydrates by obese subjects results in decreased concentrations of butyrate and butyrate-producing bacteria in feces Appl Environ Microbiol 73 1073 1078
22. PB Eckburg EM Bik CN Bernstein E Purdom L Dethlefsen, et al. 2005 Diversity of the human intestinal microbial flora Science 308 1635 1638
23. SJ Engle I Ormsby S Pawlowski GP Boivin J Croft, et al. 2002 Elimination of colon cancer in germ-free transforming growth factor beta 1-deficient mice Cancer Res 62 6362 6366
24. SE Erdman VP Rao T Poutahidis AB Rogers CL Taylor, et al. 2009 Nitric oxide and TNF-alpha trigger colonic inflammation and carcinogenesis in Helicobacter hepaticus-infected, Rag2-deficient mice Proc Natl Acad Sci USA 106 1027 1032
25. HJ Flint SH Duncan KP Scott P Louis 2007 Interactions and competition within the microbial community of the human colon: links between diet and health Environ Microbiol 9 1101 1111
26. DN Frank AL St Amand RA Feldman EC Boedeker N Harpaz, et al. 2007 Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases Proc Natl Acad Sci USA 104 13780 13785
27. A Gawronska P Dziechciarz A Horvath H Szajewska 2007 A randomized double-blind placebo-controlled trial of Lactobacillus GG abdominal pain disorders in children Aliment Pharmacol Ther 25 177 184
28. Z Ge Y Feng NS Taylor M Ohtani MF Polz, et al. 2006 Colonization dynamics of altered Schaedler flora is influenced by gender, aging, and Helicobacter hepaticus infection in the intestines of Swiss Webster mice Appl Environ Microbiol 72 5100 5103
29. SR Gill M Pop RT Deboy PB Eckburg PJ Turnbaugh, et al. 2006 Metagenomic analysis of the human distal gut microbiome Science 312 1355 1359
30. R Goodacre 2007 Metabolomics of a superorganism J Nutr 137 259S 266S
31. M Gotteland S Cruchet S Verbeke 2001 Effect of Lactobacillus ingestion on the gastrointestinal mucosal barrier alterations induced by indometacin in humans Aliment Pharmacol Ther 15 11 17
32. EA Grice HH Kong S Conlan CB Deming J Davis, et al. 2009 Topographical and temporal diversity of the human skin microbiome Science 324 1190 1192
33. D Guyonnet O Chassany P Ducrotte C Picard M Mouret, et al. 2007 Effect of a fermented milk containing Bifidobacterium animalis DN-173 010 on the health-related quality of life and symptoms in irritable bowel syndrome in adults in primary care: a multicentre, randomized, double-blind, controlled trial Aliment Pharmacol Ther 26 475 486
34. H Hayashi R Takahashi T Nishi M Sakamoto Y Benno 2005 Molecular analysis of jejunal, ileal, caecal and recto-sigmoidal human colonic microbiota using 16S rRNA gene libraries and terminal restriction fragment length polymorphism J Med Microbiol 54 1093 1101
35. HG Heilig EG Zoetendal EE Vaughan P Marteau AD Akkermans, et al. 2002 Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA Appl Environ Microbiol 68 114 123 (Pubitemid 34036493)
36. A Kassinen L Krogius-Kurikka H Makivuokko T Rinttila L Paulin, et al. 2007 The fecal microbiota of irritable bowel syndrome patients differs significantly from that of healthy subjects Gastroenterology 133 24 33
37. R Kuhn J Lohler D Rennick K Rajewsky W Muller 1993 Interleukin-10- deficient mice develop chronic enterocolitis Cell 75 263 274
38. K Kurokawa T Itoh T Kuwahara K Oshima H Toh, et al. 2007 Comparative metagenomics revealed commonly enriched gene sets in human gut microbiomes DNA Res 14 169 181
39. J Lederberg 2000 Infectious history Science 288 287 293
40. RE Ley F Backhed P Turnbaugh CA Lozupone RD Knight, et al. 2005 Obesity alters gut microbial ecology Proc Natl Acad Sci USA 102 11070 11075
41. RE Ley DA Peterson JI Gordon 2006 Ecological and evolutionary forces shaping microbial diversity in the human intestine Cell 124 837 848
42. RE Ley M Hamady C Lozupone PJ Turnbaugh RR Ramey, et al. 2008 Evolution of mammals and their gut microbes Science 320 1647 1651
43. M Li B Wang M Zhang M Rantalainen S Wang, et al. 2008 Symbiotic gut microbes modulate human metabolic phenotypes Proc Natl Acad Sci USA 105 2117 2122
44. T Liebregts B Adam C Bredack A Roth S Heinzel, et al. 2007 Immune activation in patients with irritable bowel syndrome Gastroenterology 132 913 920
45. B Linz F Balloux Y Moodley A Manica H Liu, et al. 2007 An African origin for the intimate association between humans and Helicobacter pylori Nature 445 915 918
46. L Maggio-Price P Treuting W Zeng M Tsang H Bielefeldt-Ohmann, et al. 2006 Heliobacter infection is required for inflammation and colon cancer in SMAD3-deficient mice Cancer Res 66 828 838
47. D Mariat O Firmesse F Levenez VD Guimaraes H Sokol, et al. 2009 The Firmicutes/Bacteroides ratio of the human microbiota changes with age BMC Microbiol 9 123
48. FP Martin ME Dumas Y Wang C Legido-Quigley IK Yap, et al. 2007 A top-down systems biology view of microbiome-mammalian metabolic interactions in a mouse model Mol Syst Biol 3 112
49. I Martinez G Wallace C Zhang R Legge AK Benson, et al. 2009 Diet-induced metabolic improvements in a hamster model of hypercholesterolemia are strongly linked to alterations of the gut microbiota Appl Environ Microbiol 75 4175 4184
50. SK Mazmanian CH Liu AO Tzianabos DL Kasper 2005 An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system Cell 122 107 118
51. W Meinl S Sczesny R Brigelius-Flohe M Blaut H Glatt 2009 Impact of gut microbiota on intestinal and hepatic levels of phase 2 xenobiotic-metabolizing enzymes in the rat Drug Metab Dispos 37 1179 1186
52. Metchnikoff E (1908) The prolongation of life: optimistic studies. G. P. Putnam's Sons, New York
53. I Nasidze J Li D Quinque K Tang M Stoneking 2009 Global diversity in the human salivary microbiome Genome Res 19 636 643
54. AW Nicholls RJ Mortishire-Smith JK Nicholson 2003 NMR spectroscopic-based metabonomic studies of urinary metabolite variation in acclimatizing germ-free rats Chem Res Toxicol 16 1395 1404
55. Nones K, Knoch B, Dommels YE, Paturi G, Butts C et al (2009) Multidrug resistance gene deficient (mdr1a (-/-)) mice have an altered caecal microbiota that precedes the onset of intestinal inflammation. J Appl Microbiol [Epub ahead of print]
56. MC Noverr NR Falkowski RA McDonald AN McKenzie GB Huffnagle 2005 Development of allergic airway disease in mice following antibiotic therapy and fungal microbiota increase: role of host genetics, antigen, and interleukin-13 Infect Immun 73 30 38
57. SJ O'Keefe D Chung N Mahmoud AR Sepulveda M Manafe, et al. 2007 Why do African Americans get more colon cancer than Native Africans? J Nutr 137 175S 182S
58. L O'Mahony M Feeney S O'Halloran L Murphy B Kiely, et al. 2001 Probiotic impact on microbial flora, inflammation and tumour development in IL-10 knockout mice Aliment Pharmacol Ther 15 1219 1225
59. L O'Mahony J McCarthy P Kelly G Hurley F Luo, et al. 2005 Lactobacillus and bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles Gastroenterology 128 541 551
60. JM Ordovas V Mooser 2006 Metagenomics: the role of the microbiome in cardiovascular disease Curr Opin Lipidol 17 157 161
61. AC Ouwehand S Salminen E Isolauri 2002 Probiotics: an overview of beneficial effects Antonie Van Leeuwenhoek 82 279 289
62. HM Parracho MO Bingham GR Gibson AL McCartney 2005 Differences between the gut microbiota of children with autistic spectrum disorders and that of healthy children J Med Microbiol 54 987 991
63. L Peran D Camuesco M Comalada A Nieto A Concha, et al. 2005 Preventative effects of a probiotic, Lactobacillus salivarius ssp. salivarius, in the TNBS model of rat colitis World J Gastroenterol 11 5185 5192
64. RD Pridmore B Berger F Desiere D Vilanova C Barretto, et al. 2004 The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533 Proc Natl Acad Sci USA 101 2512 2517
65. Prisciandaro L, Geier M, Butler R, Cummins A, Howarth G (2009) Probiotics and their derivatives as treatments for inflammatory bowel disease. Inflamm Bowel Dis [Epub ahead of print]
66. SE Pryde SH Duncan GL Hold CS Stewart HJ Flint 2002 The microbiology of butyrate formation in the human colon FEMS Microbiol Lett 217 133 139
67. EM Quigley 2006 Germs, gas and the gut; the evolving role of the enteric flora in IBS Am J Gastroenterol 101 334 335
68. T Rankinen A Zuberi YC Chagnon SJ Weisnagel G Argyropoulos, et al. 2006 The human obesity gene map: the 2005 update Obesity (Silver Spring) 14 529 644
69. VP Rao T Poutahidis Z Ge PR Nambiar C Boussahmain, et al. 2006 Innate immune inflammatory response against enteric bacteria Helicobacter hepaticus induces mammary adenocarcinoma in mice Cancer Res 66 7395 7400
70. Y Ringel AD Sperber DA Drossman 2001 Irritable bowel syndrome Annu Rev Med 52 319 338
71. IR Rowland AK Mallett A Wise 1985 The effect of diet on the mammalian gut flora and its metabolic activities Crit Rev Toxicol 16 31 103
72. RB Sarma-Rupavtarm Z Ge DB Schauer JG Fox MF Polz 2004 Spatial distribution and stability of the eight microbial species of the altered schaedler flora in the mouse gastrointestinal tract Appl Environ Microbiol 70 2791 2800
73. RB Sartor 1997 The influence of normal microbial flora on the development of chronic mucosal inflammation Res Immunol 148 567 576
74. JF Seegers 2002 Lactobacilli as live vaccine delivery vectors: progress and prospects Trends Biotechnol 20 508 515
75. DA Sela J Chapman A Adeuya JH Kim F Chen, et al. 2008 The genome sequence of Bifidobacterium longum subsp. infantis reveals adaptations for milk utilization within the infant microbiome Proc Natl Acad Sci USA 105 18964 18969
76. A Shreiner GB Huffnagle MC Noverr 2008 The "Microbiota Hypothesis" of allergic disease Adv Exp Med Biol 635 113 134
77. L Steidler W Hans L Schotte S Neirynck F Obermeier, et al. 2000 Treatment of murine colitis by Lactococcus lactis secreting interleukin-10 Science 289 1352 1355
78. JA Stewart VS Chadwick A Murray 2005 Investigations into the influence of host genetics on the predominant eubacteria in the faecal microbiota of children J Med Microbiol 54 1239 1242
79. J Swann Y Wang L Abecia A Costabile K Tuohy, et al. 2009 Gut microbiome modulates the toxicity of hydrazine: a metabonomic study Mol Biosyst 5 351 355
80. NJ Talley 2006 Irritable bowel syndrome Intern Med J 36 724 728
81. GW Tannock K Munro HJ Harmsen GW Welling J Smart, et al. 2000 Analysis of the fecal microbiota of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20 Appl Environ Microbiol 66 2578 2588
82. GR Thompson PC Trexler 1971 Gastrointestinal structure and function in germ-free or gnotobiotic animals Gut 12 230 235
83. RY Tito S Macmil G Wiley F Najar L Cleeland, et al. 2008 Phylotyping and functional analysis of two ancient human microbiomes PLoS ONE 3 e3703
84. PJ Turnbaugh RE Ley MA Mahowald V Magrini ER Mardis, et al. 2006 An obesity-associated gut microbiome with increased capacity for energy harvest Nature 444 1027 1031
85. PJ Turnbaugh RE Ley M Hamady CM Fraser-Liggett R Knight, et al. 2007 The human microbiome project Nature 449 804 810
86. PJ Turnbaugh F Backhed L Fulton JI Gordon 2008 Diet-induced obesity is linked to marked but reversible alterations in the mouse distal gut microbiome Cell Host Microbe 3 213 223
87. PJ Turnbaugh M Hamady T Yatsunenko BL Cantarel A Duncan, et al. 2009 A core gut microbiome in obese and lean twins Nature 457 480 484
88. JM Uronis M Muhlbauer HH Herfarth TC Rubinas GS Jones, et al. 2009 Modulation of the intestinal microbiota alters colitis-associated colorectal cancer susceptibility PLoS ONE 4 e6026
89. JP Van de Merwe JH Stegeman MP Hazenberg 1983 The resident faecal flora is determined by genetic characteristics of the host. Implications for Crohn's disease? Antonie Van Leeuwenhoek 49 119 124
90. K Vandenbroucke W Hans J Van Huysse S Neirynck P Demetter, et al. 2004 Active delivery of trefoil factors by genetically modified Lactococcus lactis prevents and heals acute colitis in mice Gastroenterology 127 502 513
91. G Vinderola C Matar G Perdigon 2005 Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: involvement of toll-like receptors Clin Diagn Lab Immunol 12 1075 1084
92. WB Whitman DC Coleman WJ Wiebe 1998 Prokaryotes: the unseen majority Proc Natl Acad Sci USA 95 6578 6583
93. WR Wikoff AT Anfora J Liu PG Schultz SA Lesley, et al. 2008 Metabolomics analysis reveals large effects of gut microbiota on mammalian blood metabolites Proc Natl Acad Sci USA 106 3698 3703
94. J Xu MK Bjursell J Himrod S Deng LK Carmichael, et al. 2003 A genomic view of the human-Bacteroides thetaiotaomicron symbiosis Science 299 2074 2076
95. J Xu MA Mahowald RE Ley CA Lozupone M Hamady, et al. 2007 Evolution of symbiotic bacteria in the distal human intestine PLoS Biol 5 e156
96. Zhou X, Westman R, Hickey R, Hansmann MA, Kennedy C et al (2009) Vaginal microbiota of women with frequent vulvovaginal candidiasis. Infect Immun [Epub ahead of print]
97. EG Zoetendal ADL Akkermans WM Akkermans-van Vliet JAGM de Visser WM de Vos 2001 The host genotype affects the bacterial community in the human gastrointestinal tract Microb Ecol Health Dis 13 129 134