Skip to main content
SpringerLink
Log in

The Symbiotic Self

  • Synthesis Paper
  • Published:
Evolutionary Biology Aims and scope Submit manuscript

Abstract

The classical one genome-one organism conception of the individual is yielding today to a symbiotic conception of the organism. Microbial symbiosis is fundamental in our evolution, physiology and development. This notion, while not new, has been revitalized by advances in molecular methods for studying microbial diversity over the past decade. An ecological understanding of our microbial communities in health and disease supplements the venerable one germ-one disease conception of classical germ theory, and reinforces the view that nothing in biology makes sense except in light of symbiosis.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Balter, M. (2012). Taking stock of the human microbiome and disease. Science, 8(2012), 1246–1247.

    Article  Google Scholar 

  • Bell, P. J. (2001). Viral eukaryogenesis: Was the ancestor of the nucleus a complex DNA Virus? Journal of Molecular Evolution, 53, 251–256.

    Article  CAS  PubMed  Google Scholar 

  • Bhat, A. K. (2013). Preserving microbial diversity of soil ecosystem: A key to sustainable productivity. International Journal of Current Microbial and Applied Science, 2, 85–101.

    Google Scholar 

  • Björkholm, B., et al. (2009). Intestinal microbiota regulate xenobiotic metabolism in the liver. PLoS ONE, 4, e6958.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bollinger, R. R., Barbas, A. S., Bush, E. L., Lin, S. S., & Parker, W. (2007). Biofilms in the large bowel suggest an apparent function of the human veriform appendix. Journal of Theoretical Biology, 249(2007), 826–831.

    Article  CAS  Google Scholar 

  • Bordenstein, S. R., & Theis, K. R. (2015). Host biology in light of the microbiome: Ten principles of holobionts and hologenomes. PLoS Biology, 13, e1002226.

    Article  PubMed  PubMed Central  Google Scholar 

  • Claverie, J. M. (2006). Viruses take center stage in cellular evolution. Genome Biology, 7, 110. doi:10.1186/gb-2006-7-6-110).

    Article  PubMed  PubMed Central  Google Scholar 

  • Costello, E. (2012a). The application of ecological theory toward an understanding of the human microbiome. Science, 336, 1255–1262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Costello, Elizabeth. (2012b). The Application of ecological theory toward an understanding of the human microbiome. Science, 336, 1255–1262.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couzin-Frankel, J. (2010). Bacteria and asthma: Untangling the links. Science, 26, 1168–1169.

    Article  Google Scholar 

  • De Bary, A. (1879). Die Erscheinung der Symbiose, Vortrag auf der Versammlung der Naturforsher und Aertze zu Cassel (pp. 1–30). Strassburg: Verlag von Karl F. Trubner.

    Google Scholar 

  • d’Herelle, F. (1926). The Bacteriophage and its behaviour. Translated by George H. Smith (p. 320). Baltimore: Williams and Wilkins.

    Book  Google Scholar 

  • Dubos, R. (1961). Integrative and creative aspects of infection. In M. Pollard (Ed.), Perspectives in virology (Vol. 2, pp. 200–205). Minneapolis: Burgess Publishing.

    Google Scholar 

  • Dunning Hotopp, J. C., Clark, M. E., Oliviera, D. C., Foster, J. M., Fisher, P., et al. (2007). Widespread lateral gene transfer from intracellular bacteria to multicellular eukaryotes. Science, 317, 1753–1756.

    Article  CAS  PubMed  Google Scholar 

  • East, E. M. (1934). The nucleus-plasma problem. American Naturalist, 68, 402–439.

    Article  Google Scholar 

  • Gontier N ed (2015) Reticulated evolution: Symbiogenesis, lateral gene transfer, hybridization and infectious heredity. Springer International.

  • Finegold, S. M., et al. (2002). Gastrointestinal microflora studies in late-onset autism. Clinical Infectious Diseases, 35(Suppl 1), S6–S16.

    Article  PubMed  Google Scholar 

  • Gast, R. J., Sanders, R. W., & Caron, D. A. (2009). Ecological strategies of protists and their symbiotic relationships with prokaryotic microbes. Trends in Microbiology, 17, 563–569.

    Article  CAS  PubMed  Google Scholar 

  • Gilbert, S., Sapp, J., & Tauber, A. (2012). A symbiotic view of life: We have never been individuals. Quarterly Review of Biology, 87, 325–341.

    Article  PubMed  Google Scholar 

  • Gordon, J. (2012). Honor thy gut symbionts redux. Science, 336, 1251–1253.

    Article  CAS  PubMed  Google Scholar 

  • Gould, S. J. (1989). Wonderful life: The Burgess shale and the nature of history. London: Hutchison Radius.

    Google Scholar 

  • Gregory, F. G. (1951). A discussion on symbiosis involving micro-organisms. Proceedings of the Royal Society of London B, 139, 202–203.

    Article  Google Scholar 

  • Harmit, S. M. (2012). Retroviruses push the Envelope for Mammalian Placentation. Proceedings of the National Academy of Sciences USA, 109, 2184–2185.

    Article  Google Scholar 

  • Hartman, H., & Feerov, A. (2002). The origin of the eukaryotic cell: A genomic investigation. Proceedings of the National Academy of Sciences USA, 99, 1420–1425.

    Article  CAS  Google Scholar 

  • Herre, E. A., Mejía, L. C., Kyllo, D. A., Rojas, E., Maynard, Z., Butler, A., et al. (2007). Ecological implications of anti-pathogen effects of tropical fungal endophytes and mycorrhizae. Ecology, 88(3), 550–558.

    Article  PubMed  Google Scholar 

  • Horie, M. (2010). Endogenous non-retroviral RNA virus elements in mammalian Genomes. Nature, 463(2010), 84–87.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hsiao, E. E. Y., McBride, S. W., Hsein, S., Sharon, G., Hyde, E. R., et al. (2013). Microbiota modulate behavioral and physiological abnormalities associated with neurodevelopmental disorders. Cell, 155, 1451–1463.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, Y. J., Sethi, S., Murphy, T., Nariya, S., Boushey, H. A., & Lynch, S. V. (2014). Airway microbiome dynamics in exacerbations of chronic obstructive pulmonary disease. Journal of Clinical Microbiology, 52(8), 2813–2823.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang, D.-W., Park, J. G., Ilhan, Z. E., Wallstrom, G., LaBaer, J., et al. (2013). Reduced Incidence of Prevotella and other fermenters in intestinal microflora of autistic Children. PLoS ONE, 8(7), e68322.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knowlton, N., & Jackson, J. B. C. (2008). Shifting baselines, local impacts, and global change on coral reefs. PLoS Biology, 6(2), e54.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lederberg J. (1952). Cell genetics and hereditary symbiosis. Physiological Reviews, 32, 403–430.

    CAS  PubMed  Google Scholar 

  • Lederberg, J., & McCray, A. T. (2001). Ome Sweet ‘Omics—A genealogical treasury of words. The Scientist, 15, 8.

    Google Scholar 

  • Lee, Y. K., & Mazmanian, S. K. (2010). Has the microbiota played a critical role in the evolution of the adaptive immune system? Science, 330, 1768–1773.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ley, R. E. (2010). Obesity and the human microbiome. Current Opinion in Gastroenterology, 26, 5–11.

    Article  PubMed  Google Scholar 

  • Ley, R. E., Peterson, D. A., & Gordon, J. I. (2006). Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell, 124, 837–848.

    Article  CAS  PubMed  Google Scholar 

  • Mangan, S., Herre, E. A., & Bever, J. D. (2010). Specificity between neotropical tree seedlings and their fungal mutualists leads to plant-soil feedback. Ecology, 9, 2594–2603; 2602.

    Article  Google Scholar 

  • Marcobal, A., & Sonnenburg, J. L. (2012). Human milk oligosaccharide consumption by intestinal microbiota. Clinical Microbiology and Infection, 18, 12–15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Margulis, L. (1970). The origin of the eukaryotic cell. New Haven: Yale University Press.

    Google Scholar 

  • Margulis, L. (1991). Symbiogenesis and symbionticisim. Margulis L, and Fester R. Symbiosis as a source of evolutionary innovation (pp. 1–14). Cambridge: The MIT Press.

    Google Scholar 

  • Maynard Smith J, Szathmáry E. (1999) The origins of life. From the birth of life to the origin of language. Oxford: Oxford University Press.

    Google Scholar 

  • McFall-Ngai, M. (2002). Unseen forces: The influence of bacteria on animal development. Developmental Biology, 224, 1–14.

    Article  Google Scholar 

  • Mi, S., Lee, X., Li, X., Veldman, et al. (2000). Syncytin is a captive retroviral envelope protein involved in human placental morphogenesis. Nature, 403(6771), 785–789.

    Article  CAS  PubMed  Google Scholar 

  • Moran, N. A., & Sloan, D. B. (2015). The hologenome concept: Helpful or hollow? PLoS Biology, 13, e1002311.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pauling, L., & Zuckerkandl, E. (1965). Chemical paleogenetics: Molecular restoration studies of extinct forms of life. Acta Chemica Scandinavica, 17, 9–16.

    Google Scholar 

  • Portier, P. (1918). Les symbiotes. Paris: Masson.

    Google Scholar 

  • Quin, J. J., Li, Y., Cai, Z., Li, S., Zhu, J., et al. (2012). A Metagenome-wide association study of gut microbiota in type 2 diabetes. Nature, 490, 55–60.

    Article  Google Scholar 

  • Reshef, L., Koren, O., Lya, Y., Zilber-Rosenberg, I., & Rosenburg, E. (2006). The coral probiotic hypothesis. Environmental Microbiology, 8, 2068–2073.

    Article  CAS  PubMed  Google Scholar 

  • Rosenberg, E., & Ziber-Rosenberg, I. (2013). The hologenome concept: Human, animal and plant microbiota. Switzerland: Springer.

    Book  Google Scholar 

  • Russell, C. M., Bouvaine, S., Newell, P., & Douglas, A. E. (2013). Shared metabolic pathways in a coevolved insect-bacterial symbiosis. Applied Environmental Microbiology, 79, 6117–6123.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Samuelsson, A., Hibberd, M. L., Forssberg, H., & Pettersson, S. (2011). Normal gut microbiota modulates brain development and behavior. Proceedings of the National Academy of Sciences USA, 108, 3047–3052.

    Article  Google Scholar 

  • Sapp, J. (1994). Evolution by association. A history of symbiosis. New York: Oxford University Press.

    Google Scholar 

  • Sapp, J. (1998). Freewheeling centrioles. History and Philosophy of the Life Sciences, 20, 255–290.

    CAS  PubMed  Google Scholar 

  • Sapp, J. (2009). The new foundations of evolution. On the tree of life. New York: Oxford University Press.

    Google Scholar 

  • Schwabe, R. F., & Jobin, C. (2013). The microbome and cancer. Nature Reviews Cancer, 13, 800–812.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stanier, R.Y. (1971). Toward an evolutionary taxonomy of the bacteria. In P Miravete and D. Peláez, (Eds.) Recent advances in microbiology, international congress for microbiology, Mexico Vol 7, 595–604.

  • Syvanen, M. (1985). Cross-species transfer: Implications for a new theory of evolution. Journal of Theoretical Biology, 112, 333–343.

    Article  CAS  PubMed  Google Scholar 

  • Taylor, M. J., Bandi, C., & Hoerauf, A. (2005). Wolbachia bacterial endosymbionts of filarial nematodes. Advances in Parasitology, 60, 245–284.

    Article  PubMed  Google Scholar 

  • Theis, et al. (2016). Getting the hologenome concept right: An eco-evolutionary framework for hosts and their microbiomes, In press. 2016.

  • Thorton, H. G. (1951). Introduction. The symbiosis between rhizobium and leguminous plants and the influence on this of the bacterial Strain. Proceedings of the Royal Society of London B, 139, 171–185.

    Google Scholar 

  • Turnbaugh, P. J., & Gordon, J. I. (2009). The core gut microbiome, energy balance and obesity. Journal of Physiology, 587, 4153–4158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vartoukian, S., Palmer, R. M., & Wade, W. (2010). Strategies for culture of the unculturable bacteria. FEMS Microbial Letters, 309, 1–7.

    CAS  Google Scholar 

  • Villarreal, L., & Ryan, F. (2011). Viruses in host evolution: General principles and future extrapolations. Current Topics in Virology, 9, 79–90.

    CAS  Google Scholar 

  • Warren, J., Laura Baldo, L., & Clark, M. (2008). Wolbachia: Master manipulators of invertebrate biology. Nature Reviews, 6, 741–751.

    Google Scholar 

  • Wilson, E. B. (1925). The cell in development and heredity. New York: Macmillan.

    Google Scholar 

  • Woese, C. R., Kandler, O., & Wheelis, M. (1990). Towards a natural system of organisms: Proposal for the domains Archaea, bacteria, and eucarya. Proceedings of the National Academy of Sciences USA, 87, 4576–4579.

    Article  CAS  Google Scholar 

  • Zilber-Rosenberg, I., & Rosenberg, E. (2008). Role of microorganisms in the evolution of animals and plants: The hologenome theory of evolution. FEMS Microbial Reviews, 32, 723–735.

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The author would like to thank the Richard Lounsbery Foundation for support of his work.

Author information

Authors and Affiliations

  1. Department of Biology, Faculty of Science, York University, Toronto, M3J1P3, Canada

    Jan Sapp

Authors
  1. Jan Sapp
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jan Sapp.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Sapp, J. The Symbiotic Self. Evol Biol 43, 596–603 (2016). https://doi.org/10.1007/s11692-016-9378-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11692-016-9378-3

Keywords

Search

Navigation