期刊论文详细信息
BMC Microbiology
Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota
Michael T Bailey5  Mark Lyte3  Purnima S Kumar7  Jens Walter1  Scot E Dowd2  Zhongtang Yu6  Michael C Nelson4  Jeffrey D Galley8 
[1] Departments of Agricultural, Food & Nutritional Science and of Biological Sciences, University of Alberta, Edmonton, Canada;Molecular Research Mr DNA Laboratory, Shallowater, USA;Department of Immunotherapeutics and Biotechnology, School of Pharmacy, Texas Tech University Health Sciences Center, Abilene, USA;Department of Molecular and Cell Biology, University of Connecticut, Storrs, USA;Department of Pediatrics, Wexner Medical Center, The Ohio State University, Columbus, USA;Department of Animal Sciences, The Ohio State University, Columbus, USA;Division of Periodontology, College of Dentistry, The Ohio State University, Columbus, USA;Biosciences Division, College of Dentistry, The Ohio State University, Columbus, USA
关键词: Dysbiosis;    Lactobacillus reuteri;    Lactobacillus;    Gastrointestinal microbiota;    Psychological stress;   
Others  :  1140755
DOI  :  10.1186/1471-2180-14-189
 received in 2014-04-29, accepted in 2014-06-30,  发布年份 2014
PDF
【 摘 要 】

Background

The microbiota of the mammalian gastrointestinal (GI) tract consists of diverse populations of commensal bacteria that interact with host physiological function. Dysregulating these populations, through exogenous means such as antibiotics or dietary changes, can have adverse consequences on the health of the host. Studies from laboratories such as ours have demonstrated that exposure to psychological stressors disrupts the population profile of intestinal microbiota. To date, such studies have primarily focused on prolonged stressors (repeated across several days) and have assessed fecal bacterial populations. It is not known whether shorter stressors can also impact the microbiota, and whether colonic mucosa-associated populations can also be affected. The mucosa-associated microbiota exist in close proximity to elements of the host immune system and the two are tightly interrelated. Therefore, alterations in these populations should be emphasized. Additionally, stressors can induce differential responses in anxiety-like behavior and corticosterone outputs in variant strains of mice. Thus, whether stressor exposure can have contrasting effects on the colonic microbiota in inbred C57BL/6 mice and outbred CD-1 mice was also examined.

Results

In the present study, we used high throughput pyrosequencing to assess the effects of a single 2-hour exposure to a social stressor, called social disruption (SDR), on colonic mucosa-associated microbial profiles of C57BL/6 mice. The data indicate that exposure to the stressor significantly changed the community profile and significantly reduced the relative proportions of two genera and one family of highly abundant intestinal bacteria, including the genus Lactobacillus. This finding was confirmed using a quantitative real-time polymerase chain reaction (qPCR) technique. The use of qPCR also identified mouse strain-specific differences in bacterial abundances. L. reuteri, an immunomodulatory species, was decreased in stressor-exposed CD-1 mice, but not C57BL/6 mice.

Conclusions

These data illustrate that stressor exposure can affect microbial populations, including the lactobacilli, that are closely associated with the colonic mucosa. Because the lactobacilli can have beneficial effects on human health, stressor-induced reductions of their population could have important health implications.

【 授权许可】

   
2014 Galley et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150325103131996.pdf 389KB PDF download
Figure 4. 23KB Image download
Figure 3. 30KB Image download
Figure 2. 22KB Image download
Figure 1. 18KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】
  • [1]Turnbaugh PJ, Ley RE, Hamady M, Fraser-Liggett CM, Knight R, Gordon JI: The human microbiome project. Nature 2007, 449(7164):804-810.
  • [2]Lozupone CA, Stombaugh J, Gonzalez A, Ackermann G, Wendel D, Vazquez-Baeza Y, Jansson JK, Gordon JI, Knight R: Meta-analyses of studies of the human microbiota. Genome Res 2013, 23(10):1704-1714.
  • [3]Reinhardt C, Bergentall M, Greiner TU, Schaffner F, Ostergren-Lunden G, Petersen LC, Ruf W, Backhed F: Tissue factor and PAR1 promote microbiota-induced intestinal vascular remodelling. Nature 2012, 483(7391):627-631.
  • [4]Backhed F, Ding H, Wang T, Hooper LV, Koh GY, Nagy A, Semenkovich CF, Gordon JI: The gut microbiota as an environmental factor that regulates fat storage. Proc Natl Acad Sci U S A 2004, 101(44):15718-15723.
  • [5]Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI: Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001, 291(5505):881-884.
  • [6]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: Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011, 331(6015):337-341.
  • [7]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: Temporal and spatial interplay of microbiota and intestinal mucosa drive establishment of immune homeostasis in conventionalized mice. Mucosal Immunol 2012, 5(5):567-579.
  • [8]Williams AM, Probert CS, Stepankova R, Tlaskalova-Hogenova H, Phillips A, Bland PW: Effects of microflora on the neonatal development of gut mucosal T cells and myeloid cells in the mouse. Immunology 2006, 119(4):470-478.
  • [9]Rehman A, Sina C, Gavrilova O, Hasler R, Ott S, Baines JF, Schreiber S, Rosenstiel P: Nod2 is essential for temporal development of intestinal microbial communities. Gut 2011, 60(10):1354-1362.
  • [10]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: NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J Clin Invest 2013, 123(2):700-711.
  • [11]Xu J, Gordon JI: Honor thy symbionts. Proc Natl Acad Sci U S A 2003, 100(18):10452-10459.
  • [12]Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA: Diversity of the human intestinal microbial flora. Science 2005, 308(5728):1635-1638.
  • [13]Ley RE, Backhed F, Turnbaugh P, Lozupone CA, Knight RD, Gordon JI: Obesity alters gut microbial ecology. Proc Natl Acad Sci U S A 2005, 102(31):11070-11075.
  • [14]Nava GM, Friedrichsen HJ, Stappenbeck TS: Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J 2011, 5(4):627-638.
  • [15]Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M: Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 2011, 25(3):397-407.
  • [16]Turnbaugh PJ, Ley RE, Mahowald MA, Magrini V, Mardis ER, Gordon JI: An obesity-associated gut microbiome with increased capacity for energy harvest. Nature 2006, 444(7122):1027-1031.
  • [17]Chang JY, Antonopoulos DA, Kalra A, Tonelli A, Khalife WT, Schmidt TM, Young VB: Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis 2008, 197(3):435-438.
  • [18]Sekirov I, Tam NM, Jogova M, Robertson ML, Li Y, Lupp C, Finlay BB: Antibiotic-induced perturbations of the intestinal microbiota alter host susceptibility to enteric infection. Infect Immun 2008, 76(10):4726-4736.
  • [19]Bailey MT, Coe CL: Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 1999, 35(2):146-155.
  • [20]Mackos AR, Eubank TD, Parry NM, Bailey MT: Probiotic Lactobacillus reuteri attenuates the stressor-enhanced severity of Citrobacter rodentium infection. Infect Immun 2013, 81(9):3253-3263.
  • [21]Schreiber O, Petersson J, Phillipson M, Perry M, Roos S, Holm L: Lactobacillus reuteri prevents colitis by reducing P-selectin-associated leukocyte- and platelet-endothelial cell interactions. Am J Physiol Gastrointest Liver Physiol 2009, 296(3):G534-G542.
  • [22]Barouei J, Moussavi M, Hodgson DM: Effect of maternal probiotic intervention on HPA axis, immunity and gut microbiota in a rat model of irritable bowel syndrome. PLoS One 2012, 7(10):e46051.
  • [23]Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M: Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 2010, 78(4):1509-1519.
  • [24]Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF: Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Brain Behav Immun 2012, 26(7):1150-1159.
  • [25]Bernstein CN, Singh S, Graff LA, Walker JR, Miller N, Cheang M: A prospective population-based study of triggers of symptomatic flares in IBD. Am J Gastroenterol 2010, 105(9):1994-2002.
  • [26]Dickhaus B, Mayer EA, Firooz N, Stains J, Conde F, Olivas TI, Fass R, Chang L, Mayer M, Naliboff BD: Irritable bowel syndrome patients show enhanced modulation of visceral perception by auditory stress. Am J Gastroenterol 2003, 98(1):135-143.
  • [27]Lee KJ, Tack J: Altered intestinal microbiota in irritable bowel syndrome. Neurogastroenterol Motil 2010, 22(5):493-498.
  • [28]Sekirov I, Russell SL, Antunes LC, Finlay BB: Gut microbiota in health and disease. Physiol Rev 2010, 90(3):859-904.
  • [29]Sartor RB: Microbial influences in inflammatory bowel diseases. Gastroenterology 2008, 134(2):577-594.
  • [30]Garrett WS, Lord GM, Punit S, Lugo-Villarino G, Mazmanian SK, Ito S, Glickman JN, Glimcher LH: Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007, 131(1):33-45.
  • [31]Bailey MT, Lubach GR, Coe CL: Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 2004, 38(4):414-421.
  • [32]Carroll IM, Chang YH, Park J, Sartor RB, Ringel Y: Luminal and mucosal-associated intestinal microbiota in patients with diarrhea-predominant irritable bowel syndrome. Gut pathogens 2010, 2(1):19.
  • [33]Bajaj JS, Hylemon PB, Ridlon JM, Heuman DM, Daita K, White MB, Monteith P, Noble NA, Sikaroodi M, Gillevet PM: Colonic mucosal microbiome differs from stool microbiome in cirrhosis and hepatic encephalopathy and is linked to cognition and inflammation. Am J Physiol Gastrointest Liver Physiol 2012, 303(6):G675-G685.
  • [34]Van den Abbeele P, Van de Wiele T, Verstraete W, Possemiers S: The host selects mucosal and luminal associations of coevolved gut microorganisms: a novel concept. FEMS Microbiol Rev 2011, 35(4):681-704.
  • [35]Knowles SR, Nelson EA, Palombo EA: Investigating the role of perceived stress on bacterial flora activity and salivary cortisol secretion: a possible mechanism underlying susceptibility to illness. Biol Psychol 2008, 77(2):132-137.
  • [36]Tannock GW, Savage DC: Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infect Immun 1974, 9(3):591-598.
  • [37]Friswell MK, Gika H, Stratford IJ, Theodoridis G, Telfer B, Wilson ID, McBain AJ: Site and strain-specific variation in gut microbiota profiles and metabolism in experimental mice. PLoS One 2010, 5(1):e8584.
  • [38]Hildebrand F, Nguyen TL, Brinkman B, Yunta RG, Cauwe B, Vandenabeele P, Liston A, Raes J: Inflammation-associated enterotypes, host genotype, cage and inter-individual effects drive gut microbiota variation in common laboratory mice. Genome Biol 2013, 14(1):R4.
  • [39]Bouwknecht JA, Paylor R: Behavioral and physiological mouse assays for anxiety: a survey in nine mouse strains. Behav Brain Res 2002, 136(2):489-501.
  • [40]Julio-Pieper M, O'Mahony CM, Clarke G, Bravo JA, Dinan TG, Cryan JF: Chronic stress-induced alterations in mouse colonic 5-HT and defecation responses are strain dependent. Stress 2012, 15(2):218-226.
  • [41]Jang SE, Hyam SR, Han MJ, Kim SY, Lee BG, Kim DH: 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. J Appl Microbiol 2013, 115(3):888-896.
  • [42]Cuevas M, Flores I, Thompson KJ, Ramos-Ortolaza DL, Torres-Reveron A, Appleyard CB: Stress exacerbates endometriosis manifestations and inflammatory parameters in an animal model. Reprod Sci 2012, 19(8):851-862.
  • [43]Hoffmann C, Hill DA, Minkah N, Kirn T, Troy A, Artis D, Bushman F: Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing. Infect Immun 2009, 77(10):4668-4678.
  • [44]Craven M, Egan CE, Dowd SE, McDonough SP, Dogan B, Denkers EY, Bowman D, Scherl EJ, Simpson KW: Inflammation drives dysbiosis and bacterial invasion in murine models of ileal Crohn's disease. PLoS One 2012, 7(7):e41594.
  • [45]Lupp C, Robertson ML, Wickham ME, Sekirov I, Champion OL, Gaynor EC, Finlay BB: Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007, 2(2):119-129.
  • [46]Collins SM, McHugh K, Jacobson K, Khan I, Riddell R, Murase K, Weingarten HP: Previous inflammation alters the response of the rat colon to stress. Gastroenterology 1996, 111(6):1509-1515.
  • [47]Quan N, Avitsur R, Stark JL, He L, Lai W, Dhabhar F, Sheridan JF: Molecular mechanisms of glucocorticoid resistance in splenocytes of socially stressed male mice. J Neuroimmunol 2003, 137(1–2):51-58.
  • [48]Kinsey SG, Bailey MT, Sheridan JF, Padgett DA, Avitsur R: Repeated social defeat causes increased anxiety-like behavior and alters splenocyte function in C57BL/6 and CD-1 mice. Brain Behav Immun 2007, 21(4):458-466.
  • [49]Mays JW, Bailey MT, Hunzeker JT, Powell ND, Papenfuss T, Karlsson EA, Padgett DA, Sheridan JF: Influenza virus-specific immunological memory is enhanced by repeated social defeat. J Immunol 2010, 184(4):2014-2025.
  • [50]Bangsgaard Bendtsen KM, Krych L, Sorensen DB, Pang W, Nielsen DS, Josefsen K, Hansen LH, Sorensen SJ, Hansen AK: Gut microbiota composition is correlated to grid floor induced stress and behavior in the BALB/c mouse. PLoS One 2012, 7(10):e46231.
  • [51]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: Stress-induced corticotropin-releasing hormone-mediated NLRP6 inflammasome inhibition and transmissible enteritis in mice. Gastroenterology 2013, 144(7):1478-1487. 1487 e1471-1478
  • [52]Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, von Bergen M, McCoy KD, Macpherson AJ, Danska JS: Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science 2013, 339(6123):1084-1088.
  • [53]Park AJ, Collins J, Blennerhassett PA, Ghia JE, Verdu EF, Bercik P, Collins SM: Altered colonic function and microbiota profile in a mouse model of chronic depression. Neurogastroenterol Motil 2013, 25(9):733-e575.
  • [54]Greene BR, Blanchard EB, Wan CK: Long-term monitoring of psychosocial stress and symptomatology in inflammatory bowel disease. Behav Res Ther 1994, 32(2):217-226.
  • [55]Bennett EJ, Tennant CC, Piesse C, Badcock CA, Kellow JE: Level of chronic life stress predicts clinical outcome in irritable bowel syndrome. Gut 1998, 43(2):256-261.
  • [56]Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, Wekerle H, Krishnamoorthy G: Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature 2011, 479(7374):538-541.
  • [57]Buljevac D, Hop WC, Reedeker W, Janssens AC, van der Meche FG, van Doorn PA, Hintzen RQ: Self reported stressful life events and exacerbations in multiple sclerosis: prospective study. BMJ 2003, 327(7416):646.
  • [58]Allen RG, Lafuse WP, Powell ND, Webster Marketon JI, Stiner-Jones LM, Sheridan JF, Bailey MT: Stressor-induced increase in microbicidal activity of splenic macrophages is dependent upon peroxynitrite production. Infect Immun 2012, 80(10):3429-3437.
  • [59]Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG, Edrington TS: Evaluation of the bacterial diversity in the feces of cattle using 16S rDNA bacterial tag-encoded FLX amplicon pyrosequencing (bTEFAP). BMC Microbiol 2008, 8:125.
  • [60]Callaway TR, Dowd SE, Edrington TS, Anderson RC, Krueger N, Bauer N, Kononoff PJ, Nisbet DJ: 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. J Anim Sci 2010, 88(12):3977-3983.
  • [61]Williams WL, Tedeschi LO, Kononoff PJ, Callaway TR, Dowd SE, Karges K, Gibson ML: Evaluation of in vitro gas production and rumen bacterial populations fermenting corn milling (co)products. J Dairy Sci 2010, 93(10):4735-4743.
  • [62]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: QIIME allows analysis of high-throughput community sequencing data. Nat Methods 2010, 7(5):335-336.
  • [63]Edgar RC: Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010, 26(19):2460-2461.
  • [64]DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, Huber T, Dalevi D, Hu P, Andersen GL: Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol 2006, 72(7):5069-5072.
  • [65]Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R: PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 2010, 26(2):266-267.
  • [66]Wang Q, Garrity GM, Tiedje JM, Cole JR: Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 2007, 73(16):5261-5267.
  • [67]Price MN, Dehal PS, Arkin AP: FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 2010, 5(3):e9490.
  • [68]Chen J, Yu Z, Michel FC Jr, Wittum T, Morrison M: 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. Appl Environ Microbiol 2007, 73(14):4407-4416.
  • [69]Anderson K, Yu Z, Chen J, Jenkins J, Courtney P, Morrison M: Analyses of Bifidobacterium, Lactobacillus, and total bacterial populations in healthy volunteers consuming calcium gluconate by denaturing gradient gel electrophoresis and real-time PCR. Int J Probiotics Prebiotics 2008, 3:31-36.
  • [70]Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP: Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol 2001, 67(6):2578-2585.
  • [71]Heilig HG, Zoetendal EG, Vaughan EE, Marteau P, Akkermans AD, de Vos WM: 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 2002, 68(1):114-123.
  • [72]Rinttila T, Kassinen A, Malinen E, Krogius L, Palva A: Development of an extensive set of 16S rDNA-targeted primers for quantification of pathogenic and indigenous bacteria in faecal samples by real-time PCR. J Appl Microbiol 2004, 97(6):1166-1177.
  • [73]Brisbin JT, Gong J, Orouji S, Esufali J, Mallick AI, Parvizi P, Shewen PE, Sharif S: Oral treatment of chickens with lactobacilli influences elicitation of immune responses. Clin Vaccine Immunol 2011, 18(9):1447-1455.
  • [74]Tong J, Liu C, Summanen P, Xu H, Finegold SM: Application of quantitative real-time PCR for rapid identification of Bacteroides fragilis group and related organisms in human wound samples. Anaerobe 2011, 17(2):64-68.
  • [75]Head CC, Farrow MJ, Sheridan JF, Padgett DA: Androstenediol reduces the anti-inflammatory effects of restraint stress during wound healing. Brain Behav Immun 2006, 20(6):590-596.
  • [76]Allen RG, Lafuse WP, Galley JD, Ali MM, Ahmer BM, Bailey MT: The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. 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]Lozupone C, Knight R: UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 2005, 71(12):8228-8235.
  • [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.
  文献评价指标  
  下载次数:14次 浏览次数:23次