Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The resilience of the intestinal microbiota influences health and disease

Nature Reviews Microbiology volume 15, pages 630–638 (2017)Cite this article

Subjects

Abstract

The composition of the intestinal microbiota varies among individuals and throughout development, and is dependent on host and environmental factors. However, although the microbiota is constantly exposed to environmental challenges, its composition and function in an individual are stable against perturbations, as microbial communities are resilient and resistant to change. The maintenance of a beneficial microbiota requires a homeostatic equilibrium within microbial communities, and also between the microorganisms and the intestinal interface of the host. The resilience of the healthy microbiota protects us from dysbiosis-related diseases, such as inflammatory bowel disease (IBD) or metabolic disorder. By contrast, a resilient dysbiotic microbiota may cause disease. In this Opinion article, we propose that microbial resilience has a key role in health and disease. We will discuss the concepts and mechanisms of microbial resilience against dietary, antibiotic or bacteriotherapy-induced perturbations and the implications for human health.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Get just this article for as long as you need it

$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematic representation of resilience phenomena in health and disease.
Figure 2: Conceptual elements that govern the stability of the intestinal ecosystem.
Figure 3: Mechanisms of resilience.
Figure 4: Faecal microbiota transplantation as a perturbation to a resilient dysbiotic community.

References

  1. Human Microbiome Project Consortium. Structure, function and diversity of the healthy human microbiome. Nature 486, 207–214 (2012).

  2. Qin, J. et al. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464, 59–65 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Faith, J. J. et al. The long-term stability of the human gut microbiota. Science 341, 1237439 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Caporaso, J. G. et al. Moving pictures of the human microbiome. Genome Biol. 12, R50 (2011).

    Article  PubMed  PubMed Central  Google Scholar 

  5. Walker, B., Holling, C. S., Carpenter, S. R. & Kinzig, A. Resilience, adaptability and transformability in social–ecological systems. Ecol. Soc. 9, 5 (2004).

    Article  Google Scholar 

  6. Moya, A. & Ferrer, M. Functional redundancy-induced stability of gut microbiota subjected to disturbance. Trends Microbiol. 24, 402–413 (2016).

    Article  CAS  PubMed  Google Scholar 

  7. Lozupone, C. A., Stombaugh, J. I., Gordon, J. I., Jansson, J. K. & Knight, R. Diversity, stability and resilience of the human gut microbiota. Nature 489, 220–230 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Greenhalgh, K., Meyer, K. M., Aagaard, K. M. & Wilmes, P. The human gut microbiome in health: establishment and resilience of microbiota over a lifetime. Environ. Microbiol. 18, 2103–2116 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  9. Chassaing, B. et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519, 92–96 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Suez, J. et al. Artificial sweeteners induce glucose intolerance by altering the gut microbiota. Nature 514, 181–186 (2014).

    Article  CAS  PubMed  Google Scholar 

  11. Henle, J. in Pathologische Untersuchungen 1–82 (Hirschwald, 1840).

  12. Koch, R. Die Ätiologie der Tuberkulose [German]. Berliner Klinische Wochenschrift 19, 428–445 (1882).

    Google Scholar 

  13. Singh, V. P., Proctor, S. D. & Willing, B. P. Koch's postulates, microbial dysbiosis and inflammatory bowel disease. Clin. Microbiol. Infect. 22, 594–599 (2016).

    Article  CAS  PubMed  Google Scholar 

  14. Shade, A. et al. Fundamentals of microbial community resistance and resilience. Front. Microbiol. 3, 417 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  15. Bender, E. A., Case, T. J. & Gilpin, M. E. Perturbation experiments in community ecology: theory and practice. Ecology 65, 1–13 (1984).

    Article  Google Scholar 

  16. Oliver, T. H. et al. Biodiversity and resilience of ecosystem functions. Trends Ecol. Evol. 30, 673–684 (2015).

    Article  PubMed  Google Scholar 

  17. Gunderson, L. H. Ecological resilience — in theory and application. Annu. Rev. Ecol. Syst. 31, 425–439 (2000).

    Article  Google Scholar 

  18. Holling, C. S. & Gunderson, L. in Panarchy: Understanding Transformations in Human and Natural Systems 25–62 (Island Press, 2002).

  19. Holling, C. S. Resilience and stability of ecological systems. Annu. Rev. Ecol. Syst. 4, 1–23 (1973).

    Article  Google Scholar 

  20. Sommer, F. & Backhed, F. Know your neighbor: microbiota and host epithelial cells interact locally to control intestinal function and physiology. Bioessays 38, 455–464 (2016).

    Article  PubMed  Google Scholar 

  21. Wang, J. et al. Dietary history contributes to enterotype-like clustering and functional metagenomic content in the intestinal microbiome of wild mice. Proc. Natl Acad. Sci. USA 111, E2703–E2710 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. David, L. A. et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 505, 559–563 (2014).

    Article  CAS  PubMed  Google Scholar 

  23. McNaughton, S. J. Diversity and stability of ecological communities: a comment on the role of empiricism in ecology. Am. Nat. 111, 515–525 (1977).

    Article  Google Scholar 

  24. Naeem, S. & Li, S. Biodiversity enhances ecosystem reliability. Nature 390, 507–509 (1997).

    Article  CAS  Google Scholar 

  25. Ley, R. E., Turnbaugh, P. J., Klein, S. & Gordon, J. I. Microbial ecology: human gut microbes associated with obesity. Nature 444, 1022–1023 (2006).

    Article  CAS  PubMed  Google Scholar 

  26. Turnbaugh, P. J. et al. A core gut microbiome in obese and lean twins. Nature 457, 480–484 (2009).

    Article  CAS  PubMed  Google Scholar 

  27. Ley, R. E. et al. Obesity alters gut microbial ecology. Proc. Natl Acad. Sci. USA 102, 11070–11075 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Furet, J. P. et al. Differential adaptation of human gut microbiota to bariatric surgery-induced weight loss: links with metabolic and low-grade inflammation markers. Diabetes 59, 3049–3057 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Manichanh, C. et al. Reduced diversity of faecal microbiota in Crohn's disease revealed by a metagenomic approach. Gut 55, 205–211 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Willing, B. P. et al. A pyrosequencing study in twins shows that gastrointestinal microbial profiles vary with inflammatory bowel disease phenotypes. Gastroenterology 139, 1844–1854.e1 (2010).

    Article  PubMed  Google Scholar 

  31. Ott, S. J. et al. Reduction in diversity of the colonic mucosa associated bacterial microflora in patients with active inflammatory bowel disease. Gut 53, 685–693 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Lepage, P. et al. Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 141, 227–236 (2011).

    Article  PubMed  Google Scholar 

  33. Chang, J. Y. et al. Decreased diversity of the fecal microbiome in recurrent Clostridium difficile-associated diarrhea. J. Infect. Dis. 197, 435–438 (2008).

    Article  PubMed  Google Scholar 

  34. Arumugam, M. et al. Enterotypes of the human gut microbiome. Nature 473, 174–180 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Zhernakova, A. et al. Population-based metagenomics analysis reveals markers for gut microbiome composition and diversity. Science 352, 565–569 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Moeller, A. H. et al. Chimpanzees and humans harbour compositionally similar gut enterotypes. Nat. Commun. 3, 1179 (2012).

    Article  CAS  PubMed  Google Scholar 

  37. Horst, K. et al. Risk stratification by injury distribution in polytrauma patients — does the clavicular fracture play a role? Patient Saf. Surg. 7, 23 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  38. Wu, G. D. et al. Linking long-term dietary patterns with gut microbial enterotypes. Science 334, 105–108 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Vieira-Silva, S. et al. Species–function relationships shape ecological properties of the human gut microbiome. Nat. Microbiol. 1, 16088 (2016).

    Article  CAS  PubMed  Google Scholar 

  40. Schreiber, S., Rosenstiel, P., Albrecht, M., Hampe, J. & Krawczak, M. Genetics of Crohn disease, an archetypal inflammatory barrier disease. Nat. Rev. Genet. 6, 376–388 (2005).

    Article  CAS  PubMed  Google Scholar 

  41. Hsiao, A. et al. Members of the human gut microbiota involved in recovery from Vibrio cholerae infection. Nature 515, 423–426 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Schwab, C. et al. Longitudinal study of murine microbiota activity and interactions with the host during acute inflammation and recovery. ISME J. 8, 1101–1114 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Buffie, C. G. et al. Profound alterations of intestinal microbiota following a single dose of clindamycin results in sustained susceptibility to Clostridium difficile-induced colitis. Infect. Immun. 80, 62–73 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Nemergut, D. R. et al. Patterns and processes of microbial community assembly. Microbiol. Mol. Biol. Rev. 77, 342–356 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  45. Seedorf, H. et al. Bacteria from diverse habitats colonize and compete in the mouse gut. Cell 159, 253–266 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Salzman, N. H. et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat. Immunol. 11, 76–83 (2010).

    Article  CAS  PubMed  Google Scholar 

  47. Sommer, F. et al. Altered mucus glycosylation in core 1 O-glycan-deficient mice affects microbiota composition and intestinal architecture. PLoS ONE 9, e85254 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Johansson, M. E. et al. The inner of the two Muc2 mucin-dependent mucus layers in colon is devoid of bacteria. Proc. Natl Acad. Sci. USA 105, 15064–15069 (2008).

    Article  PubMed  PubMed Central  Google Scholar 

  49. Hooper, L. V., Littman, D. R. & Macpherson, A. J. Interactions between the microbiota and the immune system. Science 336, 1268–1273 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Wehkamp, J. et al. Reduced Paneth cell α-defensins in ileal Crohn's disease. Proc. Natl Acad. Sci. USA 102, 18129–18134 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Mathewson, N. D. et al. Gut microbiome-derived metabolites modulate intestinal epithelial cell damage and mitigate graft-versus-host disease. Nat. Immunol. 17, 505–513 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Nigro, G., Rossi, R., Commere, P. H., Jay, P. & Sansonetti, P. J. The cytosolic bacterial peptidoglycan sensor Nod2 affords stem cell protection and links microbes to gut epithelial regeneration. Cell Host Microbe 15, 792–798 (2014).

    Article  CAS  PubMed  Google Scholar 

  53. Lindemans, C. A. et al. Interleukin-22 promotes intestinal-stem-cell-mediated epithelial regeneration. Nature 528, 560–564 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hadizadeh, F. et al. Stool frequency is associated with gut microbiota composition. Gut 66, 559–560 (2016).

    Article  PubMed  Google Scholar 

  55. Falony, G. et al. Population-level analysis of gut microbiome variation. Science 352, 560–564 (2016).

    Article  CAS  PubMed  Google Scholar 

  56. Alam, A. et al. The microenvironment of injured murine gut elicits a local pro-restitutive microbiota. Nat. Microbiol. 1, 15021 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Pedron, T. et al. A crypt-specific core microbiota resides in the mouse colon. mBio 3, e00116-12 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  58. Gillilland, M. G. III et al. Ecological succession of bacterial communities during conventionalization of germ-free mice. Appl. Environ. Microbiol. 78, 2359–2366 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Wier, A. M. et al. Transcriptional patterns in both host and bacterium underlie a daily rhythm of anatomical and metabolic change in a beneficial symbiosis. Proc. Natl Acad. Sci. USA 107, 2259–2264 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  60. Sender, R., Fuchs, S. & Milo, R. Revised estimates for the number of human and bacteria cells in the body. PLoS Biol. 14, e1002533 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Thaiss, C. A. et al. Transkingdom control of microbiota diurnal oscillations promotes metabolic homeostasis. Cell 159, 514–529 (2014).

    Article  CAS  PubMed  Google Scholar 

  62. Thaiss, C. A. et al. Microbiota diurnal rhythmicity programs host transcriptome oscillations. Cell 167, 1495–1510.e12 (2016).

    Article  CAS  PubMed  Google Scholar 

  63. Faust, K. & Raes, J. Microbial interactions: from networks to models. Nat. Rev. Microbiol. 10, 538–550 (2012).

    Article  CAS  PubMed  Google Scholar 

  64. Jones, S. E. & Lennon, J. T. Dormancy contributes to the maintenance of microbial diversity. Proc. Natl Acad. Sci. USA 107, 5881–5886 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  65. Pedros-Alio, C. Marine microbial diversity: can it be determined? Trends Microbiol. 14, 257–263 (2006).

    Article  CAS  PubMed  Google Scholar 

  66. Lennon, J. T. & Jones, S. E. Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat. Rev. Microbiol. 9, 119–130 (2011).

    Article  CAS  PubMed  Google Scholar 

  67. Tait, K. & Sutherland, I. W. Antagonistic interactions amongst bacteriocin-producing enteric bacteria in dual species biofilms. J. Appl. Microbiol. 93, 345–352 (2002).

    Article  CAS  PubMed  Google Scholar 

  68. LaSarre, B. & Federle, M. J. Exploiting quorum sensing to confuse bacterial pathogens. Microbiol. Mol. Biol. Rev. 77, 73–111 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Tan, C. H. et al. Community quorum sensing signalling and quenching: microbial granular biofilm assembly. NPJ Biofilms Microbiomes 1, 15006 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  70. Dominguez-Bello, M. G. et al. Delivery mode shapes the acquisition and structure of the initial microbiota across multiple body habitats in newborns. Proc. Natl Acad. Sci. USA 107, 11971–11975 (2010).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Sommer, F. & Backhed, F. The gut microbiota — masters of host development and physiology. Nat. Rev. Microbiol. 11, 227–238 (2013).

    Article  CAS  PubMed  Google Scholar 

  72. Rehman, A. et al. Nod2 is essential for temporal development of intestinal microbial communities. Gut 60, 1354–1362 (2011).

    Article  CAS  PubMed  Google Scholar 

  73. Rakoff-Nahoum, S. et al. Analysis of gene–environment interactions in postnatal development of the mammalian intestine. Proc. Natl Acad. Sci. USA 112, 1929–1936 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Koenig, J. E. et al. Succession of microbial consortia in the developing infant gut microbiome. Proc. Natl Acad. Sci. USA 108 (Suppl. 1), 4578–4585 (2011).

    Article  PubMed  Google Scholar 

  75. Palmer, C., Bik, E. M., DiGiulio, D. B., Relman, D. A. & Brown, P. O. Development of the human infant intestinal microbiota. PLoS Biol. 5, e177 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Yatsunenko, T. et al. Human gut microbiome viewed across age and geography. Nature 486, 222–227 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Russell, S. L. et al. Early life antibiotic-driven changes in microbiota enhance susceptibility to allergic asthma. EMBO Rep. 13, 440–447 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Dominguez-Bello, M. G. et al. Partial restoration of the microbiota of cesarean-born infants via vaginal microbial transfer. Nat. Med. 22, 250–253 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Subramanian, S. et al. Persistent gut microbiota immaturity in malnourished Bangladeshi children. Nature 510, 417–421 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Dethlefsen, L. & Relman, D. A. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc. Natl Acad. Sci. USA 108 (Suppl. 1), 4554–4561 (2011).

    Article  PubMed  Google Scholar 

  81. Heinsen, F. A. et al. Dynamic changes of the luminal and mucosa-associated gut microbiota during and after antibiotic therapy with paromomycin. Gut Microbes 6, 243–254 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Jernberg, C., Lofmark, S., Edlund, C. & Jansson, J. K. Long-term ecological impacts of antibiotic administration on the human intestinal microbiota. ISME J. 1, 56–66 (2007).

    Article  CAS  PubMed  Google Scholar 

  83. Lindner, C. et al. Diversification of memory B cells drives the continuous adaptation of secretory antibodies to gut microbiota. Nat. Immunol. 16, 880–888 (2015).

    Article  CAS  PubMed  Google Scholar 

  84. Schumann, A. et al. Neonatal antibiotic treatment alters gastrointestinal tract developmental gene expression and intestinal barrier transcriptome. Physiol. Genomics 23, 235–245 (2005).

    Article  CAS  PubMed  Google Scholar 

  85. Biedermann, L. & Rogler, G. The intestinal microbiota: its role in health and disease. Eur. J. Pediatr. 174, 151–167 (2015).

    Article  CAS  PubMed  Google Scholar 

  86. Theriot, C. M., Bowman, A. A. & Young, V. B. Antibiotic-induced alterations of the gut microbiota alter secondary bile acid production and allow for Clostridium difficile spore germination and outgrowth in the large intestine. mSphere http://dx.doi.org/10.1128/mSphere.00045-15 (2016).

  87. Risnes, K. R., Belanger, K., Murk, W. & Bracken, M. B. Antibiotic exposure by 6 months and asthma and allergy at 6 years: findings in a cohort of 1,401 US children. Am. J. Epidemiol. 173, 310–318 (2011).

    Article  PubMed  Google Scholar 

  88. Shaw, S. Y., Blanchard, J. F. & Bernstein, C. N. Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am. J. Gastroenterol. 105, 2687–2692 (2010).

    Article  PubMed  Google Scholar 

  89. Kronman, M. P., Zaoutis, T. E., Haynes, K., Feng, R. & Coffin, S. E. Antibiotic exposure and IBD development among children: a population-based cohort study. Pediatrics 130, e794–e803 (2012).

    Article  PubMed  PubMed Central  Google Scholar 

  90. Azad, M. B., Bridgman, S. L., Becker, A. B. & Kozyrskyj, A. L. Infant antibiotic exposure and the development of childhood overweight and central adiposity. Int. J. Obes. (Lond.) 38, 1290–1298 (2014).

    Article  CAS  Google Scholar 

  91. Boursi, B., Mamtani, R., Haynes, K. & Yang, Y. X. The effect of past antibiotic exposure on diabetes risk. Eur. J. Endocrinol. 172, 639–648 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Blaser, M. J. Antibiotic use and its consequences for the normal microbiome. Science 352, 544–545 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Vrieze, A. et al. Transfer of intestinal microbiota from lean donors increases insulin sensitivity in individuals with metabolic syndrome. Gastroenterology 143, 913–916.e7 (2012).

    Article  CAS  PubMed  Google Scholar 

  94. Bäckhed, F. et al. The gut microbiota as an environmental factor that regulates fat storage. Proc. Natl Acad. Sci. USA 101, 15718–15723 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Couturier-Maillard, A. et al. NOD2-mediated dysbiosis predisposes mice to transmissible colitis and colorectal cancer. J. Clin. Invest. 123, 700–711 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Vijay-Kumar, M. et al. Metabolic syndrome and altered gut microbiota in mice lacking Toll-like receptor 5. Science 328, 228–231 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Hamilton, M. J., Weingarden, A. R., Unno, T., Khoruts, A. & Sadowsky, M. J. High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes 4, 125–135 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Li, S. S. et al. Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science 352, 586–589 (2016).

    Article  CAS  PubMed  Google Scholar 

  99. Manichanh, C. et al. Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res. 20, 1411–1419 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. Fuentes, S. et al. Reset of a critically disturbed microbial ecosystem: faecal transplant in recurrent Clostridium difficile infection. ISME J. 8, 1621–1633 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  101. Grinspan, A. M. & Kelly, C. R. Fecal microbiota transplantation for ulcerative colitis: not just yet. Gastroenterology 149, 15–18 (2015).

    Article  PubMed  Google Scholar 

  102. Eiseman, B., Silen, W., Bascom, G. S. & Kauvar, A. J. Fecal enema as an adjunct in the treatment of pseudomembranous enterocolitis. Surgery 44, 854–859 (1958).

    CAS  PubMed  Google Scholar 

  103. van Nood, E. et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N. Engl. J. Med. 368, 407–415 (2013).

    Article  CAS  PubMed  Google Scholar 

  104. Broecker, F., Klumpp, J. & Moelling, K. Long-term microbiota and virome in a Zurich patient after fecal transplantation against Clostridium difficile infection. Ann. NY Acad. Sci. 1372, 29–41 (2016).

    Article  PubMed  Google Scholar 

  105. Vermeire, S. et al. Donor species richness determines faecal microbiota transplantation success in inflammatory bowel disease. J. Crohns Colitis 10, 387–394 (2016).

    Article  PubMed  Google Scholar 

  106. Colman, R. J. & Rubin, D. T. Fecal microbiota transplantation as therapy for inflammatory bowel disease: a systematic review and meta-analysis. J. Crohns Colitis 8, 1569–1581 (2014).

    Article  PubMed  Google Scholar 

  107. Moayyedi, P. et al. Fecal microbiota transplantation induces remission in patients with active ulcerative colitis in a randomized controlled trial. Gastroenterology 149, 102–109.e6 (2015).

    Article  PubMed  Google Scholar 

  108. Rossen, N. G. et al. Findings from a randomized controlled trial of fecal transplantation for patients with ulcerative colitis. Gastroenterology 149, 110–118.e4 (2015).

    Article  PubMed  Google Scholar 

  109. Ott, S. J. et al. Efficacy of sterile fecal filtrate transfer for treating patients with Clostridium difficile infection. Gastroenterology 152, 799–811.e7 (2016).

    Article  PubMed  Google Scholar 

  110. Rykiel, E. J. Towards a definition of ecological disturbance. Aust. J. Ecol. 10, 361–365 (1985).

    Article  Google Scholar 

  111. Worm, B. & Duffy, J. E. Biodiversity, productivity and stability in real food webs. Trends Ecol. Evol. 18, 628–632 (2003).

    Article  Google Scholar 

  112. Relman, D. A. The human microbiome: ecosystem resilience and health. Nutr. Rev. 70, S2–S9 (2012).

    Article  PubMed  Google Scholar 

  113. Costello, E. K. et al. Bacterial community variation in human body habitats across space and time. Science 326, 1694–1697 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. David, L. A. et al. Host lifestyle affects human microbiota on daily timescales. Genome Biol. 15, R89 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Costello, E. K., Stagaman, K., Dethlefsen, L., Bohannan, B. J. & Relman, D. A. The application of ecological theory toward an understanding of the human microbiome. Science 336, 1255–1262 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Tamboli, C. P., Neut, C., Desreumaux, P. & Colombel, J. F. Dysbiosis in inflammatory bowel disease. Gut 53, 1–4 (2004).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Deutsche Forschungsgemeinschaft (DFG; grants CRC1182 C2 and CRC877 B9), the Federal Ministry of Education and Research as part of the e:Med framework ('sysINFLAME'; grant 01ZX1306), the Cluster of Excellence 'Inflammation at Interfaces' (grant ExC 306) and SYSCID (a systems medicine approach to chronic inflammatory diseases) in the European Union's Horizon 2020 research and innovation programme under grant agreement No 733100. The authors express that this article represents an opinionated perspective rather than a systematic review. The authors apologize to those researchers whose important contribution to the field could not be cited owing to space constraints.

Author information

Authors and Affiliations

  1. Felix Sommer, Jacqueline Moltzau Anderson, Richa Bharti and Philip Rosenstiel are at the Institute of Clinical Molecular Biology, Christian Albrechts University and University Hospital Schleswig-Holstein, Campus Kiel, Rosalind-Franklin-Straße 12, 24105 Kiel, Germany.,

    Felix Sommer, Jacqueline Moltzau Anderson, Richa Bharti & Philip Rosenstiel

  2. Jeroen Raes is at the Department of Microbiology and Immunology, Belgium; and at the Department of Bioengineering Sciences, Rega Institute, KU Leuven - University of Leuven, Leuven 3000, Belgium; at the Vlaams Instituut voor Biotechnologie (VIB), Center for Microbiology, Leuven 3000, Research Group of Microbiology, Vrije Universiteit Brussel, Brussels 1050, Belgium.,

    Jeroen Raes

  3. at the Vlaams Instituut voor Biotechnologie (VIB), Center for Microbiology, Leuven 3000, Belgium,

    Jeroen Raes

Authors
  1. Felix Sommer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jacqueline Moltzau Anderson
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Richa Bharti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jeroen Raes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Philip Rosenstiel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Felix Sommer or Philip Rosenstiel.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

PowerPoint slides

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sommer, F., Anderson, J., Bharti, R. et al. The resilience of the intestinal microbiota influences health and disease. Nat Rev Microbiol 15, 630–638 (2017). https://doi.org/10.1038/nrmicro.2017.58

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrmicro.2017.58

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing