Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota

BMC Microbiology

Volumn 14, Issue 1, 2014, Pages

  Galley, Jeffrey D ^a   Nelson, Michael C ^b   Yu, Zhongtang ^a   Dowd, Scot E ^c   Walter, Jens ^d   Kumar, Purnima S ^a   Lyte, Mark ^e   Bailey, Michael T ^a,f  

^a OHIO STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CONNECTICUT   (United States)

^c Molecular Research Mr DNA Laboratory   (United States)

^d UNIVERSITY OF ALBERTA   (Canada)

^e TEXAS TECH UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^f THE OHIO STATE UNIVERSITY WEXNER MEDICAL CENTER   (United States)

Author keywords

Dysbiosis; Gastrointestinal microbiota; Lactobacillus; Lactobacillus reuteri; Psychological stress

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; COLON MUCOSA; COMMUNITY STRUCTURE; INTESTINE FLORA; LACTOBACILLUS REUTERI; MICROFLORA; MOUSE; MOUSE STRAIN; NONHUMAN; PYROSEQUENCING; REAL TIME POLYMERASE CHAIN REACTION; SOCIAL STRESS; ACETOBACTERACEAE; BACTERIA; BACTEROIDACEAE; C57BL 6 MOUSE; CD-1 MOUSE; CLOSTRIDIACEAE; CLOSTRIDIALES; COLON FLORA; CONTROLLED STUDY; ENVIRONMENTAL EXPOSURE; HIGH THROUGHPUT SEQUENCING; LACHNOSPIRACEAE; LACTOBACILLACEAE; LACTOBACILLUS; MICROBIAL COMMUNITY; PEPTOSTREPTOCOCCACEAE; PORPHYROMONADACEAE; RUMINOCOCCACEAE; SOCIAL DISRUPTION;

BACTERIA (MICROORGANISMS); LACTOBACILLUS; LACTOBACILLUS REUTERI; MAMMALIA; MUS;

ANIMALS; BIOTA; COLON; INTESTINAL MUCOSA; MALE; MICE; MICE, INBRED C57BL; STRESS, PHYSIOLOGICAL;

EID: 84904084581     PISSN: None     EISSN: 14712180     Source Type: Journal    
DOI: 10.1186/1471-2180-14-189     Document Type: Article

References (80)

1. The human microbiome project. Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI, Nature 2007 449 7164 804 810 (Pubitemid 47598620)
2. Meta-analyses of studies of the human microbiota. Lozupone CA, Stombaugh J, Gonzalez A, Ackermann G, Wendel D, Vazquez-Baeza Y, Jansson JK, Gordon JI, Knight R, Genome Res 2013 23 10 1704 1714
3. Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling. Reinhardt C, Bergentall M, Greiner TU, Schaffner F, Ostergren-Lunden G, Petersen LC, Ruf W, Backhed F, Nature 2012 483 7391 627 631
4. The gut microbiota as an environmental factor that regulates fat storage. Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI, Proc Natl Acad Sci U S A 2004 101 44 15718 15723 (Pubitemid 39473554)
5. Molecular analysis of commensal host-microbial relationships in the intestine. Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI, Science 2001 291 5505 881 884 (Pubitemid 32120760)
6. Induction of colonic regulatory T cells by indigenous Clostridium species. Atarashi K, Tanoue T, Shima T, Imaoka A, Kuwahara T, Momose Y, Cheng G, Yamasaki S, Saito T, Ohba Y, Taniguchi T, Takeda K, Hori S, Ivanov II, Umesaki Y, Itoh K, Honda K, Science 2011 331 6015 337 341
7. Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. El Aidy S, van Baarlen P, Derrien M, Lindenbergh-Kortleve DJ, Hooiveld G, Levenez F, Dore J, Dekker J, Samsom JN, Nieuwenhuis EE, Kleerebezem M, Mucosal Immunol 2012 5 5 567 579
8. Effects of microflora on the neonatal development of gut mucosal T cells and myeloid cells in the mouse. Williams AM, Probert CS, Stepankova R, Tlaskalova-Hogenova H, Phillips A, Bland PW, Immunology 2006 119 4 470 478 (Pubitemid 44722209)
9. Nod2 is essential for temporal development of intestinal microbial communities. Rehman A, Sina C, Gavrilova O, Hasler R, Ott S, Baines JF, Schreiber S, Rosenstiel P, Gut 2011 60 10 1354 1362
10. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. Couturier-Maillard A, Secher T, Rehman A, Normand S, De Arcangelis A, Haesler R, Huot L, Grandjean T, Bressenot A, Delanoye-Crespin A, Gaillot O, Schreiber S, Lemoine Y, Ryffel B, Hot D, Nùñez G, Chen G, Rosenstiel P, Chamaillard M, J Clin Invest 2013 123 2 700 711
11. Honor thy symbionts. Xu J, Gordon JI, Proc Natl Acad Sci U S A 2003 100 18 10452 10459 (Pubitemid 37071899)
12. Diversity of the human intestinal microbial flora. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA, Science 2005 308 5728 1635 1638 (Pubitemid 40807514)
13. Obesity alters gut microbial ecology. Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI, Proc Natl Acad Sci U S A 2005 102 31 11070 11075 (Pubitemid 41105994)
14. Spatial organization of intestinal microbiota in the mouse ascending colon. Nava GM, Friedrichsen HJ, Stappenbeck TS, ISME J 2011 5 4 627 638
15. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M, Brain Behav Immun 2011 25 3 397 407
16. An obesity-associated gut microbiome with increased capacity for energy harvest. Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI, Nature 2006 444 7122 1027 1031 (Pubitemid 46018515)
17. Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea. Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, Young VB, J Infect Dis 2008 197 3 435 438 (Pubitemid 351263426)
18. Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, Finlay BB, Infect Immun 2008 76 10 4726 4736
19. Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Bailey MT, Coe CL, Dev Psychobiol 1999 35 2 146 155 (Pubitemid 29416198)
20. Probiotic Lactobacillus reuteri attenuates the stressor-enhanced severity of Citrobacter rodentium infection. Mackos AR, Eubank TD, Parry NM, Bailey MT, Infect Immun 2013 81 9 3253 3263
21. Lactobacillus reuteri prevents colitis by reducing P-selectin-associated leukocyte- and platelet-endothelial cell interactions. Schreiber O, Petersson J, Phillipson M, Perry M, Roos S, Holm L, Am J Physiol Gastrointest Liver Physiol 2009 296 3 534 G542
22. Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. Barouei J, Moussavi M, Hodgson DM, PLoS One 2012 7 10 46051
23. Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M, Infect Immun 2010 78 4 1509 1519
24. Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF, Brain Behav Immun 2012 26 7 1150 1159
25. A prospective population-based study of triggers of symptomatic flares in IBD. Bernstein CN, Singh S, Graff LA, Walker JR, Miller N, Cheang M, Am J Gastroenterol 2010 105 9 1994 2002
26. Irritable bowel syndrome patients show enhanced modulation of visceral perception by auditory stress. Dickhaus B, Mayer EA, Firooz N, Stains J, Conde F, Olivas TI, Fass R, Chang L, Mayer M, Naliboff BD, Am J Gastroenterol 2003 98 1 135 143 (Pubitemid 36135182)
27. Altered intestinal microbiota in irritable bowel syndrome. Lee KJ, Tack J, Neurogastroenterol Motil 2010 22 5 493 498
28. Gut microbiota in health and disease. Sekirov I, Russell SL, Antunes LC, Finlay BB, Physiol Rev 2010 90 3 859 904
29. Microbial influences in inflammatory bowel diseases. Sartor RB, Gastroenterology 2008 134 2 577 594 (Pubitemid 351173057)
30. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH, Cell 2007 131 1 33 45 (Pubitemid 47505255)
31. Prenatal stress alters bacterial colonization of the gut in infant monkeys. Bailey MT, Lubach GR, Coe CL, J Pediatr Gastroenterol Nutr 2004 38 4 414 421
32. Luminal and mucosal-associated intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Carroll IM, Chang YH, Park J, Sartor RB, Ringel Y, Gut pathogens 2010 2 1 19
33. Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Bajaj JS, Hylemon PB, Ridlon JM, Heuman DM, Daita K, White MB, Monteith P, Noble NA, Sikaroodi M, Gillevet PM, Am J Physiol Gastrointest Liver Physiol 2012 303 6 675 G685
34. The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S, FEMS Microbiol Rev 2011 35 4 681 704
35. Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Knowles SR, Nelson EA, Palombo EA, Biol Psychol 2008 77 2 132 137
36. Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Tannock GW, Savage DC, Infect Immun 1974 9 3 591 598
37. Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. Friswell MK, Gika H, Stratford IJ, Theodoridis G, Telfer B, Wilson ID, McBain AJ, PLoS One 2010 5 1 8584
38. Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Hildebrand F, Nguyen TL, Brinkman B, Yunta RG, Cauwe B, Vandenabeele P, Liston A, Raes J, Genome Biol 2013 14 1 4
39. Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Bouwknecht JA, Paylor R, Behav Brain Res 2002 136 2 489 501 (Pubitemid 35333265)
40. Chronic stress-induced alterations in mouse colonic 5-HT and defecation responses are strain dependent. Julio-Pieper M, O'Mahony CM, Clarke G, Bravo JA, Dinan TG, Cryan JF, Stress 2012 15 2 218 226
41. Lactobacillus brevis G-101 ameliorates colitis in mice by inhibiting NF-kappaB, MAPK and AKT pathways and by polarizing M1 macrophages to M2-like macrophages. Jang SE, Hyam SR, Han MJ, Kim SY, Lee BG, Kim DH, J Appl Microbiol 2013 115 3 888 896
42. Stress exacerbates endometriosis manifestations and inflammatory parameters in an animal model. Cuevas M, Flores I, Thompson KJ, Ramos-Ortolaza DL, Torres-Reveron A, Appleyard CB, Reprod Sci 2012 19 8 851 862
43. Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing. Hoffmann C, Hill DA, Minkah N, Kirn T, Troy A, Artis D, Bushman F, Infect Immun 2009 77 10 4668 4678
44. Inflammation drives dysbiosis and bacterial invasion in murine models of ileal Crohn's disease. Craven M, Egan CE, Dowd SE, McDonough SP, Dogan B, Denkers EY, Bowman D, Scherl EJ, Simpson KW, PLoS One 2012 7 7 41594
45. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB, Cell Host Microbe 2007 2 2 119 129 (Pubitemid 47209521)
46. Previous inflammation alters the response of the rat colon to stress. Collins SM, McHugh K, Jacobson K, Khan I, Riddell R, Murase K, Weingarten HP, Gastroenterology 1996 111 6 1509 1515 (Pubitemid 26404214)
47. Molecular mechanisms of glucocorticoid resistance in splenocytes of socially stressed male mice. Quan N, Avitsur R, Stark JL, He L, Lai W, Dhabhar F, Sheridan JF, J Neuroimmunol 2003 137 1-2 51 58 (Pubitemid 36351565)
48. Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Kinsey SG, Bailey MT, Sheridan JF, Padgett DA, Avitsur R, Brain Behav Immun 2007 21 4 458 466 (Pubitemid 46546517)
49. Influenza virus-specific immunological memory is enhanced by repeated social defeat. Mays JW, Bailey MT, Hunzeker JT, Powell ND, Papenfuss T, Karlsson EA, Padgett DA, Sheridan JF, J Immunol 2010 184 4 2014 2025
50. Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. Bangsgaard Bendtsen KM, Krych L, Sorensen DB, Pang W, Nielsen DS, Josefsen K, Hansen LH, Sorensen SJ, Hansen AK, PLoS One 2012 7 10 46231
51. Stress-induced corticotropin-releasing hormone-mediated NLRP6 inflammasome inhibition and transmissible enteritis in mice. Sun Y, Zhang M, Chen CC, Gillilland M Jr, Sun X, El-Zaatari M, Huffnagle GB, Young VB, Zhang J, Hong SC, Chang YM, Gumucio DL, Owyang C, Kao JY, Gastroenterology 2013 144 7 1478 1487 1487 e1471-1478
52. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, von Bergen M, McCoy KD, Macpherson AJ, Danska JS, Science 2013 339 6123 1084 1088
53. Altered colonic function and microbiota profile in a mouse model of chronic depression. Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P, Collins SM, Neurogastroenterol Motil 2013 25 9 733 e575
54. Long-term monitoring of psychosocial stress and symptomatology in inflammatory bowel disease. Greene BR, Blanchard EB, Wan CK, Behav Res Ther 1994 32 2 217 226 (Pubitemid 24046577)
55. Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Bennett EJ, Tennant CC, Piesse C, Badcock CA, Kellow JE, Gut 1998 43 2 256 261 (Pubitemid 28348331)
56. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, Wekerle H, Krishnamoorthy G, Nature 2011 479 7374 538 541
57. Self reported stressful life events and exacerbations in multiple sclerosis: prospective study. Buljevac D, Hop WC, Reedeker W, Janssens AC, van der Meche FG, van Doorn PA, Hintzen RQ, BMJ 2003 327 7416 646
58. Stressor-induced increase in microbicidal activity of splenic macrophages is dependent upon peroxynitrite production. Allen RG, Lafuse WP, Powell ND, Webster Marketon JI, Stiner-Jones LM, Sheridan JF, Bailey MT, Infect Immun 2012 80 10 3429 3437
59. Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS, BMC Microbiol 2008 8 125
60. Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grains plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing. Callaway TR, Dowd SE, Edrington TS, Anderson RC, Krueger N, Bauer N, Kononoff PJ, Nisbet DJ, J Anim Sci 2010 88 12 3977 3983
61. Evaluation of in vitro gas production and rumen bacterial populations fermenting corn milling (co)products. Williams WL, Tedeschi LO, Kononoff PJ, Callaway TR, Dowd SE, Karges K, Gibson ML, J Dairy Sci 2010 93 10 4735 4743
62. QIIME allows analysis of high-throughput community sequencing data. Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Pena AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R, Nat Methods 2010 7 5 335 336
63. Search and clustering orders of magnitude faster than BLAST. Edgar RC, Bioinformatics 2010 26 19 2460 2461
64. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL, Appl Environ Microbiol 2006 72 7 5069 5072 (Pubitemid 44078840)
65. PyNAST: a flexible tool for aligning sequences to a template alignment. Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R, Bioinformatics 2010 26 2 266 267
66. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Wang Q, Garrity GM, Tiedje JM, Cole JR, Appl Environ Microbiol 2007 73 16 5261 5267 (Pubitemid 47326658)
67. FastTree 2-approximately maximum-likelihood trees for large alignments. Price MN, Dehal PS, Arkin AP, PLoS One 2010 5 3 9490
68. Development and application of real-time PCR assays for quantification of erm genes conferring resistance to macrolides-lincosamides-streptogramin B in livestock manure and manure management systems. Chen J, Yu Z, Michel FC Jr, Wittum T, Morrison M, Appl Environ Microbiol 2007 73 14 4407 4416 (Pubitemid 47122582)
69. Analyses of Bifidobacterium, Lactobacillus, and total bacterial populations in healthy volunteers consuming calcium gluconate by denaturing gradient gel electrophoresis and real-time PCR. Anderson K, Yu Z, Chen J, Jenkins J, Courtney P, Morrison M, Int J Probiotics Prebiotics 2008 3 31 36
70. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP, Appl Environ Microbiol 2001 67 6 2578 2585 (Pubitemid 33639729)
71. Molecular diversity of Lactobacillus spp. and other lactic acid bacteria in the human intestine as determined by specific amplification of 16S ribosomal DNA. Heilig HG, Zoetendal EG, Vaughan EE, Marteau P, Akkermans AD, de Vos WM, Appl Environ Microbiol 2002 68 1 114 123 (Pubitemid 34036493)
72. Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A, J Appl Microbiol 2004 97 6 1166 1177 (Pubitemid 39573940)
73. Oral treatment of chickens with lactobacilli influences elicitation of immune responses. Brisbin JT, Gong J, Orouji S, Esufali J, Mallick AI, Parvizi P, Shewen PE, Sharif S, Clin Vaccine Immunol 2011 18 9 1447 1455
74. Application of quantitative real-time PCR for rapid identification of Bacteroides fragilis group and related organisms in human wound samples. Tong J, Liu C, Summanen P, Xu H, Finegold SM, Anaerobe 2011 17 2 64 68
75. Androstenediol reduces the anti-inflammatory effects of restraint stress during wound healing. Head CC, Farrow MJ, Sheridan JF, Padgett DA, Brain Behav Immun 2006 20 6 590 596 (Pubitemid 44528956)
76. The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. Allen RG, Lafuse WP, Galley JD, Ali MM, Ahmer BM, Bailey MT, Brain Behav Immun 2012 26 3 371 382
77. Shannon CE, Weaver W, The mathematical theory of communication Urbana: University of Illinois Press 1949
78. UniFrac: a new phylogenetic method for comparing microbial communities. Lozupone C, Knight R, Appl Environ Microbiol 2005 71 12 8228 8235 (Pubitemid 41803949)
79. Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Henry M, Stevens HH, Wagner H, Vegan: community ecology package R package version 2.0-3 2012
80. Development Core Team, R: a language and environment for statistical computing R Foundation for Statistical Computing, Vienna, Austria. Coventry, United Kingdom R Foundation for Statistical Computing 2011