Skip to main content
SpringerLink
Log in

Effects of Stress on Commensal Microbes and Immune System Activity

  • Chapter
Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health

Part of the book series: Advances in Experimental Medicine and Biology ((MICENDO,volume 874))

Abstract

The body harbors a vast array of microbes that are collectively known as the microbiota. Increasing attention is being paid to the role of the gut microbiota in the health of the host. Gut microbial communities are relatively resistant to change, though alterations in homeostasis can also significantly change gut microbial community structure. An important factor that has been demonstrated to alter the composition of the gut microbiota is exposure to psychological stressors. And, evidence indicates that the commensal microbiota are involved in stressor-induced immunomodulation. This chapter will discuss the impact of psychosocial stress on immunity, and present evidence that stressor-induced alterations in the composition of gut microbial communities contributes to stressor-induced immunomodulation and neurobiological sequelae. Finally, the role of the microbiota in the perinatal time period will be explored, and an integrative hypothesis of the role of the microbiome in health and stress response will be proposed.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Aagaard K, Ma J, Antony KM, Ganu R, Petrosino J, Versalovic J (2014) The placenta harbors a unique microbiome. Sci Transl Med 6:237ra65

    Article  PubMed  Google Scholar 

  • Allen RG, Lafuse WP, Galley JD, Ali MM, Ahmer BM, Bailey MT (2012a) The intestinal microbiota are necessary for stressor-induced enhancement of splenic macrophage microbicidal activity. Brain Behav Immun 26:371–382

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Allen RG, Lafuse WP, Powell ND, Stiner-Jones LM, Webster Marketon JI, Sheridan JF, Bailey MT (2012b) Stressor-induced increase in microbicidal activity of splenic macrophages is dependent upon peroxynitrite production. Infect Immun 80:3429–3437

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Avitsur R, Stark JL, Dhabhar FS, Sheridan JF (2002) Social stress alters splenocyte phenotype and function. J Neuroimmunol 132:66–71

    Article  CAS  PubMed  Google Scholar 

  • Avitsur R, Kavelaars A, Heijnen C, Sheridan JF (2005) Social stress and the regulation of tumor necrosis factor-alpha secretion. Brain Behav Immun 19:311–317

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT, Coe CL (1999) Maternal separation disrupts the integrity of the intestinal microflora in infant rhesus monkeys. Dev Psychobiol 35:146–155

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT, Karaszewski JW, Lubach GR, Coe CL, Lyte M (1999) In vivo adaptation of attenuated Salmonella typhimurium results in increased growth upon exposure to norepinephrine. Physiol Behav 67:359–364

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT, Lubach GR, Coe CL (2004) Prenatal stress alters bacterial colonization of the gut in infant monkeys. J Pediatr Gastroenterol Nutr 38:414–421

    Article  PubMed  Google Scholar 

  • Bailey MT, Engler H, Sheridan JF (2006) Stress induces the translocation of cutaneous and gastrointestinal microflora to secondary lymphoid organs of C57BL/6 mice. J Neuroimmunol 171:29–37

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT, Engler H, Powell ND, Padgett DA, Sheridan JF (2007) Repeated social defeat increases the bactericidal activity of splenic macrophages through a Toll-like receptor-dependent pathway. Am J Physiol Regul Integr Comp Physiol 293:R1180–R1190

    Article  CAS  PubMed  Google Scholar 

  • Bailey MT, Kierstein S, Sharma S, Spaits M, Kinsey SG, Tliba O, Amrani Y, Sheridan JF, Panettieri RA, Haczku A (2009a) Social stress enhances allergen-induced airway inflammation in mice and inhibits corticosteroid responsiveness of cytokine production. J Immunol 182:7888–7896

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bailey MT, Kinsey SG, Padgett DA, Sheridan JF, Leblebicioglu B (2009b) Social stress enhances IL-1beta and TNF-alpha production by Porphyromonas gingivalis lipopolysaccharide-stimulated CD11b+ cells. Physiol Behav 98:351–358

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bailey MT, Dowd SE, Parry NM, Galley JD, Schauer DB, Lyte M (2010) Stressor exposure disrupts commensal microbial populations in the intestines and leads to increased colonization by Citrobacter rodentium. Infect Immun 78:1509–1519

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bailey MT, Dowd SE, Galley JD, Hufnagle AR, Allen RG, Lyte M (2011) Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun 25:397–407

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bellavance MA, Rivest S (2014) The HPA—immune axis and the immunomodulatory actions of glucocorticoids in the brain. Front Immunol 5:136

    Article  PubMed Central  PubMed  Google Scholar 

  • Berg RD (1996) The indigenous gastrointestinal microflora. Trends Microbiol 4:430–435

    Article  CAS  PubMed  Google Scholar 

  • Berg RD (1999) Bacterial translocation from the gastrointestinal tract. Adv Exp Med Biol 473:11–30

    Article  CAS  PubMed  Google Scholar 

  • Bierhaus A, Wolf J, Andrassy M, Rohleder N, Humpert PM, Petrov D, Ferstl R, VON Eynatten M, Wendt T, Rudofsky G, Joswig M, Morcos M, Schwaninger M, McEwen B, Kirschbaum C, Nawroth PP (2003) A mechanism converting psychosocial stress into mononuclear cell activation. Proc Natl Acad Sci U S A 100:1920–1925

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Boudry G, Morise A, Seve B, Huërou-Luron ILE (2011) Effect of milk formula protein content on intestinal barrier function in a porcine model of LBW neonates. Pediatr Res 69:4–9

    Article  CAS  PubMed  Google Scholar 

  • Brydon L, Steptoe A (2005) Stress-induced increases in interleukin-6 and fibrinogen predict ambulatory blood pressure at 3-year follow-up. J Hypertens 23:1001–1007

    Article  CAS  PubMed  Google Scholar 

  • Brydon L, Edwards S, Jia H, Mohamed-Ali V, Zachary I, Martin JF, Steptoe A (2005) Psychological stress activates interleukin-1beta gene expression in human mononuclear cells. Brain Behav Immun 19:540–546

    Article  CAS  PubMed  Google Scholar 

  • Brydon L, Magid K, Steptoe A (2006) Platelets, coronary heart disease, and stress. Brain Behav Immun 20:113–119

    Article  CAS  PubMed  Google Scholar 

  • Coussons-Read ME, Okun ML, Nettles CD (2007) Psychosocial stress increases inflammatory markers and alters cytokine production across pregnancy. Brain Behav Immun 21:343–350

    Article  CAS  PubMed  Google Scholar 

  • Cryan JF, Dinan TG (2012) Mind-altering microorganisms: the impact of the gut microbiota on brain and behaviour. Nat Rev Neurosci 13:701–712

    Article  CAS  PubMed  Google Scholar 

  • Digiulio DB (2012) Diversity of microbes in amniotic fluid. Semin Fetal Neonatal Med 17:2–11

    Article  PubMed  Google Scholar 

  • Dinan TG, Stanton C, Cryan JF (2013) Psychobiotics: a novel class of psychotropic. Biol Psychiatry 74:720–726

    Article  CAS  PubMed  Google Scholar 

  • Emeny RT, Zierer A, Lacruz ME, Baumert J, Herder C, Gornitzka G, Koenig W, Thorand B, Ladwig KH, Investigators K (2013) Job strain-associated inflammatory burden and long-term risk of coronary events: findings from the MONICA/KORA Augsburg case-cohort study. Psychosom Med 75:317–325

    Article  CAS  PubMed  Google Scholar 

  • Engler H, Bailey MT, Engler A, Stiner-Jones LM, Quan N, Sheridan JF (2008) Interleukin-1 receptor type 1-deficient mice fail to develop social stress-associated glucocorticoid resistance in the spleen. Psychoneuroendocrinology 33:108–117

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fernandez MF, Boris S, Barbes C (2003) Probiotic properties of human lactobacilli strains to be used in the gastrointestinal tract. J Appl Microbiol 94:449–455

    Article  CAS  PubMed  Google Scholar 

  • Freestone PP, Williams PH, Haigh RD, Maggs AF, Neal CP, Lyte M (2002) Growth stimulation of intestinal commensal Escherichia coli by catecholamines: a possible contributory factor in trauma-induced sepsis. Shock 18:465–470

    Article  PubMed  Google Scholar 

  • Freestone PP, Sandrini SM, Haigh RD, Lyte M (2008) Microbial endocrinology: how stress influences susceptibility to infection. Trends Microbiol 16:55–64

    Article  CAS  PubMed  Google Scholar 

  • Galley JD, Nelson MC, Yu Z, Dowd SE, Walter J, Kumar PS, Lyte M, Bailey MT (2014a) Exposure to a social stressor disrupts the community structure of the colonic mucosa-associated microbiota. BMC Microbiol 14:189

    Article  PubMed Central  PubMed  Google Scholar 

  • Galley JD, Yu Z, Kumar P, Dowd SE, Lyte M, Bailey MT (2014b) The structures of the colonic mucosa-associated and luminal microbial communities are distinct and differentially affected by a prolonged murine stressor. Gut Microbes 5:748–760

    Article  PubMed  Google Scholar 

  • Gareau MG, Jury J, Yang PC, Macqueen G, Perdue MH (2006) Neonatal maternal separation causes colonic dysfunction in rat pups including impaired host resistance. Pediatr Res 59:83–88

    Article  PubMed  Google Scholar 

  • Goldenberg RL, Hauth JC, Andrews WW (2000) Intrauterine infection and preterm delivery. N Engl J Med 342:1500–1507

    Article  CAS  PubMed  Google Scholar 

  • Goncalves LF, Chaiworapongsa T, Romero R (2002) Intrauterine infection and prematurity. Ment Retard Dev Disabil Res Rev 8:3–13

    Article  PubMed  Google Scholar 

  • Gordon JI, Hooper LV, Mcnevin MS, Wong M, Bry L (1997) Epithelial cell growth and differentiation. III. Promoting diversity in the intestine: conversations between the microflora, epithelium, and diffuse GALT. Am J Physiol 273:G565–G570

    CAS  PubMed  Google Scholar 

  • Goyal N, Rishi P, Shukla G (2013) Lactobacillus rhamnosus GG antagonizes Giardia intestinalis induced oxidative stress and intestinal disaccharidases: an experimental study. World J Microbiol Biotechnol 29:1049–1057

    Article  PubMed  Google Scholar 

  • Green BT, Lyte M, Chen C, Xie Y, Casey MA, Kulkarni-Narla A, Vulchanova L, Brown DR (2004) Adrenergic modulation of Escherichia coli O157:H7 adherence to the colonic mucosa. Am J Physiol Gastrointest Liver Physiol 287:G1238–G1246

    Article  CAS  PubMed  Google Scholar 

  • Gur TL, Worly BL, Bailey MT (2015) Stress and the commensal microbiota: importance in parturition and infant neurodevelopment. Front Psychiatry 6:5

    Article  PubMed Central  PubMed  Google Scholar 

  • Hanke ML, Powell ND, Stiner LM, Bailey MT, Sheridan JF (2012) Beta adrenergic blockade decreases the immunomodulatory effects of social disruption stress. Brain Behav Immun 26:1150–1159

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huth C, Thorand B, Baumert J, Kruse J, Emeny RT, Schneider A, Meisinger C, Ladwig KH (2014) Job strain as a risk factor for the onset of type 2 diabetes mellitus: findings from the MONICA/KORA Augsburg cohort study. Psychosom Med 76:562–568

    Article  PubMed  Google Scholar 

  • Kailasapathy K, Chin J (2000) Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol 78:80–88

    Article  CAS  PubMed  Google Scholar 

  • Lalles JP (2012) Long term effects of pre- and early postnatal nutrition and environment on the gut. J Anim Sci 90(Suppl 4):421–429

    Article  PubMed  Google Scholar 

  • Lozupone CA, Stombaugh JI, Gordon JI, Jansson JK, Knight R (2012) Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lyte M (2004) The biogenic amine tyramine modulates the adherence of Escherichia coli O157:H7 to intestinal mucosa. J Food Prot 67:878–883

    CAS  PubMed  Google Scholar 

  • Lyte M, Bailey MT (1997) Neuroendocrine-bacterial interactions in a neurotoxin-induced model of trauma. J Surg Res 70:195–201

    Article  CAS  PubMed  Google Scholar 

  • Lyte M, Nguyen KT (1997) Alteration of Escherichia coli O157:H7 growth and molecular fingerprint by the neuroendocrine hormone noradrenaline. Microbios 89:197–213

    CAS  PubMed  Google Scholar 

  • Mackos AR, Eubank TD, Parry NM, Bailey MT (2013) Probiotic Lactobacillus reuteri attenuates the stressor-enhanced severity of Citrobacter rodentium infection. Infect Immun 81:3253–3263

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Maslanik T, Tannura K, Mahaffey L, Loughridge AB, Beninson L, Ursell L, Greenwood BN, Knight R, Fleshner M (2012) Commensal bacteria and MAMPs are necessary for stress-induced increases in IL-1beta and IL-18 but not IL-6, IL-10 or MCP-1. PLoS One 7, e50636

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mays JW, Bailey MT, Hunzeker JT, Powell ND, Papenfuss T, Karlsson EA, Padgett DA, Sheridan JF (2010) Influenza virus-specific immunological memory is enhanced by repeated social defeat. J Immunol 184:2014–2025

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • McLaughlin KA, Conron KJ, Koenen KC, Gilman SE (2010) Childhood adversity, adult stressful life events, and risk of past-year psychiatric disorder: a test of the stress sensitization hypothesis in a population-based sample of adults. Psychol Med 40:1647–1658

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nakade Y, Tsuchida D, Fukuda H, Iwa M, Pappas TN, Takahashi T (2005) Restraint stress delays solid gastric emptying via a central CRF and peripheral sympathetic neuron in rats. Am J Physiol Regul Integr Comp Physiol 288:R427–R432

    Article  CAS  PubMed  Google Scholar 

  • Nakade Y, Fukuda H, Iwa M, Tsukamoto K, Yanagi H, Yamamura T, Mantyh C, Pappas TN, Takahashi T (2007) Restraint stress stimulates colonic motility via central corticotropin-releasing factor and peripheral 5-HT3 receptors in conscious rats. Am J Physiol Gastrointest Liver Physiol 292:G1037–G1044

    Article  CAS  PubMed  Google Scholar 

  • O’Mahony SM, Marchesi JR, Scully P, Codling C, Ceolho AM, Quigley EM, Cryan JF, Dinan TG (2009) Early life stress alters behavior, immunity, and microbiota in rats: implications for irritable bowel syndrome and psychiatric illnesses. Biol Psychiatry 65:263–267

    Article  PubMed  Google Scholar 

  • Pullinger GD, Carnell SC, Sharaff FF, VAN Diemen PM, Dziva F, Morgan E, Lyte M, Freestone PP, Stevens MP (2010) Norepinephrine augments Salmonella enterica-induced enteritis in a manner associated with increased net replication but independent of the putative adrenergic sensor kinases QseC and QseE. Infect Immun 78:372–380

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shanahan F (2002) The host-microbe interface within the gut. Best Pract Res Clin Gastroenterol 16:915–931

    Article  PubMed  Google Scholar 

  • Shapiro GD, Fraser WD, Frasch MG, Seguin JR (2013) Psychosocial stress in pregnancy and preterm birth: associations and mechanisms. J Perinat Med 41:631–645

    PubMed  Google Scholar 

  • Shichijo K, Ito M, Taniyama K, Sekine I (1993) The role of sympathetic neurons for low susceptibility to stress in gastric lesions. Life Sci 53:261–267

    Article  CAS  PubMed  Google Scholar 

  • Stark JL, Avitsur R, Padgett DA, Campbell KA, Beck FM, Sheridan JF (2001) Social stress induces glucocorticoid resistance in macrophages. Am J Physiol Regul Integr Comp Physiol 280:R1799–R1805

    CAS  PubMed  Google Scholar 

  • Stark JL, Avitsur R, Hunzeker J, Padgett DA, Sheridan JF (2002) Interleukin-6 and the development of social disruption-induced glucocorticoid resistance. J Neuroimmunol 124:9–15

    Article  CAS  PubMed  Google Scholar 

  • Stepankova R, Sinkora J, Hudcovic T, Kozakova H, Tlaskalova-Hogenova H (1998) Differences in development of lymphocyte subpopulations from gut-associated lymphatic tissue (GALT) of germfree and conventional rats: effect of aging. Folia Microbiol (Praha) 43:531–534

    Article  CAS  Google Scholar 

  • Steptoe A, Hamer M, Chida Y (2007) The effects of acute psychological stress on circulating inflammatory factors in humans: a review and meta-analysis. Brain Behav Immun 21:901–912

    Article  CAS  PubMed  Google Scholar 

  • Tannock GW, Savage DC (1974) Influences of dietary and environmental stress on microbial populations in the murine gastrointestinal tract. Infect Immun 9:591–598

    PubMed Central  CAS  PubMed  Google Scholar 

  • Thomas CM, Hong T, VAN Pijkeren JP, Hemarajata P, Trinh DV, Hu W, Britton RA, Kalkum M, Versalovic J (2012) Histamine derived from probiotic Lactobacillus reuteri suppresses TNF via modulation of PKA and ERK signaling. PLoS One 7, e31951

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Umesaki Y, Setoyama H, Matsumoto S, Okada Y (1993) Expansion of alpha beta T-cell receptor-bearing intestinal intraepithelial lymphocytes after microbial colonization in germ-free mice and its independence from thymus. Immunology 79:32–37

    PubMed Central  CAS  PubMed  Google Scholar 

  • Umesaki Y, Okada Y, Matsumoto S, Imaoka A, Setoyama H (1995) Segmented filamentous bacteria are indigenous intestinal bacteria that activate intraepithelial lymphocytes and induce MHC class II molecules and fucosyl asialo GM1 glycolipids on the small intestinal epithelial cells in the ex-germ-free mouse. Microbiol Immunol 39:555–562

    Article  CAS  PubMed  Google Scholar 

  • Wang SX, Wu WC (2005) Effects of psychological stress on small intestinal motility and bacteria and mucosa in mice. World J Gastroenterol 11:2016–2021

    Article  PubMed Central  PubMed  Google Scholar 

  • Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, Peters EC, Siuzdak G (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 106:3698–3703

    Article  PubMed Central  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychiatry and Behavioral Health, Wexner Medical Center at The Ohio State University, Columbus, OH, 43210, USA

    Tamar L. Gur M.D., Ph.D.

  2. Department of Neuroscience, Wexner Medical Center at The Ohio State University, Columbus, OH, 43210, USA

    Tamar L. Gur M.D., Ph.D.

  3. Department of Obstetrics and Gynecology, Wexner Medical Center at The Ohio State University, Columbus, OH, 43210, USA

    Tamar L. Gur M.D., Ph.D.

  4. Institute for Behavioral Medicine Research, Wexner Medical Center at The Ohio State University, 460 Medical Drive, Room 253, Columbus, OH, 43210, USA

    Tamar L. Gur M.D., Ph.D.

  5. Center for Microbial Pathogenesis, The Research Institute at Nationwide Children’s Hospital, Columbus, OH, 43205, USA

    Michael T. Bailey Ph.D.

Authors
  1. Tamar L. Gur M.D., Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Michael T. Bailey Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Tamar L. Gur M.D., Ph.D. .

Editor information

Editors and Affiliations

  1. College of Veterinary Medicine, Iowa State University, Ames, Iowa, USA

    Mark Lyte

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing AG

About this chapter

Cite this chapter

Gur, T.L., Bailey, M.T. (2016). Effects of Stress on Commensal Microbes and Immune System Activity. In: Lyte, M. (eds) Microbial Endocrinology: Interkingdom Signaling in Infectious Disease and Health. Advances in Experimental Medicine and Biology(), vol 874. Springer, Cham. https://doi.org/10.1007/978-3-319-20215-0_14

Download citation

Publish with us

Policies and ethics

Search

Navigation