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The Hydra Holobiont: A Tale of Several Symbiotic Lineages

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The Holobiont Imperative

Abstract

The personal journey of one of us (TB) toward the realization that beneficial microbes are important began in summer 2000 when Jens Schröder, a dermatologist at Kiel University, on the occasion of the inauguration of the new chair of Zoology asked if Hydra were not a good model system to investigate the biochemistry of epithelial defenses. Nobody at that time would have anticipated that this triggered the development of a novel model system in comparative and evolutionary immunology. Up to that moment, Hydra was all for examining developmental mechanisms in an evolutionary context and to uncover basic principles of pattern formation and stem cell regulation. To think of immune reactions as equally important features of an animal did not come to our mind. That evolution of a simple multicellular animal such as Hydra means both invention of developmental pathways to shape and maintain a given body plan and also to protect this body all life long, and understanding that part of that context requires understanding the biotic and abiotic environment in which Hydra evolved turned out to be enlightening and exciting. This chapter will show just how much we know about host–microbe interactions in Hydra and what these findings mean in a more general context of holobiont research.

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References

  • Becker T, Loch G, Beyer M, Zinke I, Aschenbrenner AC, Carrera P, Inhester T, Schultze JL, Hoch M (2010) FOXO-dependent regulation of innate immune homeostasis. Nature 463(7279):369–373

    Google Scholar 

  • Boehm AM, Rosenstiel P, Bosch TCG (2013) Stem cells and aging from a quasi-immortal point of view. Bioessays 35(11):994–1003

    Article  CAS  PubMed  Google Scholar 

  • Boehm AM, Hemmrich G, Khalturin K, Puchert M, Anton-Erxleben F, Wittlieb J, Klostermeier UC, Rosenstiel P, Oberg H-H, Bosch TCG (2012) FoxO is a critical regulator of stem cell maintenance and immortality in Hydra. Proc Natl Acad Sci U S A 109(48):19697–19702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bosch TCG (2012) What Hydra has to say about the role and origin of symbiotic interactions. Biol Bull 223:78–84

    PubMed  Google Scholar 

  • Bosch TCG (2013) Cnidarian-microbe interactions and the origin of innate immunity in metazoans. Ann Rev Microbiol 67:499–518

    Article  CAS  Google Scholar 

  • Bosch, TCG, Augustin R, Anton-Erxleben F, Fraune S, Hemmrich G, Zill H, Rosenstiel P, Jacobs G, Schreiber S, Leippe M, Stanisak M, Grotzinger, Jung S, Podschun R, Bartels J, Harder J, Schroder JM (2009) Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. Developmental and comparative immunology 33:559–569

    Google Scholar 

  • Chapman JA, Kirkness EF, Simakov O, Hampson SE, Mitros T, Weinmaier T, Rattei T, Balasubramanian PG, Borman J, Busam D, Disbennett K, Pfannkoch C, Sumin N, Sutton GG, Viswanathan LD, Walenz B, Goodstein DM, Hellsten U, Kawashima T, Prochnik SE, Putnam NH, Shu S, Blumberg B, Dana CE, Gee L, Kibler DF, Law L, Lindgens D, Martinez DE, Peng J, Wigge PA, Bertulat B, Guder C, Nakamura Y, Ozbek S, Watanabe H, Khalturin K, Hemmrich G, Franke A, Augustin R, Fraune S, Hayakawa E, Hayakawa S, Hirose M, Hwang JS, Ikeo K, Nishimiya-Fujisawa C, Ogura A, Takahashi T, Steinmetz PR, Zhang X, Aufschnaiter R, Eder MK, Gorny AK, Salvenmoser W, Heimberg AM, Wheeler BM, Peterson KJ, Böttger A, Tischler P, Wolf A, Gojobori T, Remington KA, Strausberg RL, Venter JC, Technau U, Hobmayer B, Bosch TC, Holstein TW, Fujisawa T, Bode HR, David CN, Rokhsar DS, Steele RE et al (2010) The dynamic genome of Hydra. Nature 464(7288):592–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Franzenburg S, Fraune S, Altrock PM, Künzel S, Baines JF, Traulsen A, Bosch TCG (2013) Bacterial colonization of Hydra hatchlings follows a robust temporal pattern. ISME J 7(4):781–790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fraune S, Augustin R, Bosch TCG (2009) Exploring host-microbe interactions in hydra. Microbe 4(10):457–462

    Google Scholar 

  • Fraune S, Franzenburg S, Augustin R, Bosch TCG (2011a) Das Prinzip Metaorganismus. BIOspektrum 17(6):634–636

    Article  Google Scholar 

  • Fraune S, Augustin R, Bosch TCG (2011b) Embryo protection in contemporary immunology: why bacteria matter. Commun Integr Biol 4:369–372

    Article  PubMed  PubMed Central  Google Scholar 

  • Fraune S, Anton-Erxleben F, Augustin R, Franzenburg S, Knop M, Schröder K, Willoweit-Ohl D, Bosch TCG (2014) Bacteria-bacteria interactions within the microbiota of the ancestral metazoan Hydra contribute to fungal resistance. ISME J 9(7):1543–1556. doi:10.1038/ismej.2014.239

    Article  PubMed  Google Scholar 

  • Habetha M, Anton-Erxleben F, Neumann K, Bosch TCG (2003) The Hydra viridis/Chlorella symbiosis. (I) Growth and sexual differentiation in polyps without symbionts. Zoology 106(2):101–108

    Article  PubMed  Google Scholar 

  • Habetha M, Bosch TCG (2005) Symbiotic Hydra express a plant-like peroxidase gene during oogenesis. J Exp Biol 208:2157–2164

    Article  CAS  PubMed  Google Scholar 

  • Nebel A, Bosch TCG (2012) Evolution of human longevity: lessons from Hydra (Editorial). Aging 4(11):730–731

    Google Scholar 

  • Rahat M (1985) Competition between chlorellae in chimeric infections of Hydra viridis: the evolution of a stable symbiosis. J Cell Sci 77:87–92

    CAS  PubMed  Google Scholar 

  • Rahat M, Reich V (1983) A comparative study of tentacle regeneration and number in symbiotic and aposymbiotic Hydra viridis: effect of Zoochlorellae. J Exp Zool 227:63–68

    Article  Google Scholar 

  • Rahat M, Reich V (1984) Intracellular infection of aposymbiotic Hydra viridis by a foreign free-living Chlorella sp.: initiation of a stable symbiosis. J Cell Sci 65:265–277

    CAS  PubMed  Google Scholar 

  • Thorington G, Margulis L (1981) Hydra viridis: transfer of metabolites between Hydra and symbiotic algae. Biol Bull 160:175–188

    Article  CAS  PubMed  Google Scholar 

  • Trembley A (1744) Mémoires, Pour Servir à l´Histoire d´un Genre de Polypes d´Eau Douce, à Bras en Frome de Cornes. Verbeek, Leiden

    Google Scholar 

  • Wittlieb J, Khalturin K, Lohmann JU, Anton-Erxleben F, Bosch TCG (2006) Transgenic Hydra allow in vivo tracking of individual stem cells during morphogenesis. Proc Natl Acad Sci U S A 103(16):6208–6211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Bosch, T.C.G., Miller, D.J. (2016). The Hydra Holobiont: A Tale of Several Symbiotic Lineages. In: The Holobiont Imperative. Springer, Vienna. https://doi.org/10.1007/978-3-7091-1896-2_7

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