Skip to main content

The Path Less Explored: Innate Immune Reactions in Cnidarians

  • Chapter

Part of the book series: Nucleic Acids and Molecular Biology ((NUCLEIC,volume 21))

The phylum Cnidaria is one of the earliest branches in the animal tree of life. Cnidarians possess most of the gene families found in bilaterians and have retained many ancestral genes that have been lost in Drosophila and Caenorhabditis elegans. Characterization of the innate immune repertoire of extant cnidarians is, therefore, of both fundamental and applied interest — it not only provides insights into the basic immunological “tool kit” of the common ancestor of all animals, but is also likely to be important in understanding human barrier disorders by describing ancient mechanisms of host/microbial interactions and the resulting evolutionary selection processes. The chapter summarizes four aspects of immunity which can be studied particularly well within cnidarians — and which may be of interest from a comparative point of view to all immunologists: intraspecies competition in sea anemones, allorecognition and cell lineage competition in the marine hydrozoan Hydractinia, antimicrobial defense reactions in Hydra and jellyfish, and symbiotic relationships in both corals and Hydra. Studies in cnidarians reveal that there is no problem in innate immunity these basal metazoans did not attempt to solve. Thus, whatever we experience with our own innate immune system, whatever we hope to learn, we will see that the cnidarians have been there before us.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   189.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   249.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   249.99
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

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Ayre DJ, Grosberg RK (2005) Behind anemone lines: factors affecting division of labour in the social cnidarian Anthopleura elegantissima. Anim Behav 70:97–110

    Article  Google Scholar 

  • Barneah O, Benayahu Y Weis VM (2006) Comparative proteomics of symbiotic and aposymbiotic juvenile soft corals. Mar Biotechnol 8:11–16

    Article  PubMed  CAS  Google Scholar 

  • Beutler B (2004) Innate immunity: an overview. Mol Immunol 40:845–859

    Article  PubMed  CAS  Google Scholar 

  • Bigger CH (1988) The role of nematocysts in anthozoan aggression. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, San Diego, pp 295–308

    Google Scholar 

  • Bigger CH, Hildemann WH (1982) Cellular defense systems of the coelenterate. In: Cohen A, Sigel S (eds) Phylogeny and ontogeny. (The reticuloendothelial system: a comprehensive treatise, vol 3) Plenum, New York, pp 59–87

    Google Scholar 

  • Bosch TCG (2007a) Symmetry breaking in stem cells of the basal metazoan Hydra. Prog Mol Subcell Biol 45:61–78

    Article  PubMed  CAS  Google Scholar 

  • Bosch TCG (2007b) Why polyps regenerate and we don’t: towards a cellular and molecular framework for Hydra regeneration. Dev Biol 303:421–433

    Article  PubMed  CAS  Google Scholar 

  • Bosch TCG, David CN (1987) Stem cells of Hydra magnipapillata can differentiate into somatic cells and germ line cells. Dev Biol 121:182–191

    Article  Google Scholar 

  • Bridge D, et al (1995) Class-level relationships in the phylum Cnidaria: molecular and morphological evidence. Mol Biol Evol 12:679–689

    PubMed  CAS  Google Scholar 

  • Brogden KA, Guthmiller JM, Salzet M, Zasloff M (2005) The nervous system and innate immunity: the neuropeptide connection. Nat Immunol 6:558–564

    PubMed  CAS  Google Scholar 

  • Buss LW (1982) Somatic cell parasitism and the evolution of somatic tissue compatibility. Proc Natl Acad Sci USA 79:5337–5341

    Article  PubMed  CAS  Google Scholar 

  • Buss LW, Grosberg RK (1990) Morphogenetic basis for phenotypic differences in hydroid competitive behavior. Nature 343:63–66

    Article  Google Scholar 

  • Buss LW, Shenk MA (1990) Hydroid allorecognition regulates competition at both the level of the colony and at the level of the cell lineage. In: Marchalonis JJ, Reinisch C (eds) Defense molecules. Liss, New York, pp 85–105

    Google Scholar 

  • Buss LW, Yund PO (1988) A comparison of modern and historical populations of the colonial hydroid Hydractinia. Ecology 69:646–654

    Article  Google Scholar 

  • Cadavid LF (2004) Self-discrimination in colonial invertebrates: genetic control of allorecognition in the hydroid Hydractinia. Dev Comp Immunol 28:871–879

    Article  PubMed  CAS  Google Scholar 

  • Cadavid LF (2005) Self/non-self discrimination in basal metazoa: genetics of allorecognition in the hydroid Hydractinia. Integr Comp Biol 45:623–630

    Article  CAS  Google Scholar 

  • Campbell RD, Bibb C (1970) Transplantation in coelenterates. Transplant Proc 2:202–211

    PubMed  CAS  Google Scholar 

  • Chadwick-Furman N, Rinkevich B (1994) A complex allorecognition system in a reef-building coral: delayed responses, reversals and nontransitive hierarchies. Coral Reefs 13:57–63

    Article  Google Scholar 

  • Cherry S, Silverman N (2006) Host–pathogen interactions in Drosophila: new tricks from an old friend. Nat Immunol 7:911–917

    Article  PubMed  CAS  Google Scholar 

  • Collins AG, et al (2006) Medusozoan phylogeny and character evolution clarified by new large and small subunit rDNA data and an assessment of the utility of phylogenetic mixture models. Syst Biol55:97–115

    Article  Google Scholar 

  • Du Pasquier L (1974) The genetic control of histocompatibility reactions: phylogenetic aspects. Arch Biol 85:91–103

    CAS  Google Scholar 

  • Du Pasquier L (2001) The immune system of invertebrates and vertebrates (review). Comp Biochem Physiol B Biochem Mol Biol 129:1–15

    Article  PubMed  CAS  Google Scholar 

  • Dunn SR, Thomason JC, Le Tissier MD, Bythell JC (2004) Heat stress induces different forms of cell death in sea anemones and their endosymbiotic algae depending on temperature and duration. Cell Death Differ 11:1213–1222

    Article  PubMed  CAS  Google Scholar 

  • Durham F (1888) On the emigration of ameboid corpuscles in the starfish. Proc R Soc Lond B 43:328–330

    Google Scholar 

  • Frank U, Rinkevich B (1994) Nontransitive patterns of historecognition phenomena in the Red Sea hydrocoral Millepora dichotoma. Mar Biol 118:723–729

    Article  Google Scholar 

  • Fujita T (2002) Evolution of the lectin-complement pathway and its role in innate immunity (review). Nat Rev Immunol 2:346–353

    Article  PubMed  CAS  Google Scholar 

  • Gravato-Nobre MJ, Hodgkin J (2005) Caenorhabditis elegans as a model for innate immunity to pathogens (review). Cell Microbiol 7:741–751

    Article  PubMed  CAS  Google Scholar 

  • Grosberg RK, Hartt MW, Levitan DR (1997) Is allorecognition specificity in Hydractinia symbiolongicarpus controlled by a single gene? Genetics 145:857–860

    PubMed  CAS  Google Scholar 

  • Habetha M, Bosch TCG (2005) Symbiotic Hydra express a plant-like peroxidase gene during oogenesis. J Exp Biol 208:2157–2165

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Hartog JC den (1977) The marginal tentacles of Rhodactissanctithomae (Corallimorphia) and the sweeper tentacles of Monrastrea cavernosa (Scleractinia): their cnidom and possible function. Proc Int Coral Reef Symp 3:463–469

    Google Scholar 

  • Hauenschild VC (1954) Genetische und entwichlungphysiologische Untersuchungen ueber Intersexualitaet und Gewebevertraeglichkeit bei Hydractinia echinata Flem. Wilhelm Roux Arch Entwicklungsmech Org 147:1–41

    Article  Google Scholar 

  • Hauenschild VC (1956) Uber die Vererbung einer Gewebevertraeglichkeitseigenschaft bei dem Hydroidpolypen Hydractinia echinata. Z Naturforsch 1956:132–138

    Google Scholar 

  • Hemmrich G, Miller DJ, Bosch TCG (2007) The evolution of immunity – a low life perspective. Trends Immunol (in press)

    Google Scholar 

  • Hildemann WH, Jokiel PL, Bigger CH, Johnston IS (1980) Allogeneic polymorphism and alloimmune memory in the coral, Montipora verrucosa.Transplantation 30:297–301

    Article  PubMed  CAS  Google Scholar 

  • Ivker FB (1972) A hierarchy of histo-compatibility in Hydractinia echinata. Biol Bull 143:162–174

    Article  Google Scholar 

  • Kasahara S, Bosch TCG (2003) Enhanced antibacterial activity in Hydra polyps lacking nerve cells. Dev Comp Immunol 27:79–166

    Article  PubMed  Google Scholar 

  • Kass-Simon AA, Scappaticci AA (2002) The behavioral and developmental physiology of nematocysts. Can J Zool 80:1772–1794

    Article  Google Scholar 

  • Khalturin K, Bosch TCG (2006) Self/nonself discrimination at the basis of chordate evolution: limits on molecular conservation. Curr Opin Immunol 19:4–9

    Article  PubMed  CAS  Google Scholar 

  • Khalturin K, Panzer Z, Cooper MD, Bosch TCG (2004) Recognition strategies in the innate immune system of ancestral chordates. Mol Immunol 41:1077–1087

    Article  PubMed  CAS  Google Scholar 

  • Kim DH, Ausubel FM (2005) Evolutionary perspectives on innate immunity from the study of Caenorhabditis elegans (review). Curr Opin Immunol 17:4–10

    Article  PubMed  CAS  Google Scholar 

  • Kusserow A, et al (2005) Unexpected complexity of the Wnt gene family in a sea anemone. Nature 433:156–160

    Article  PubMed  CAS  Google Scholar 

  • Lang J (1973) Interspecific aggression by scleractinian corals. 2. Whythe race is not only to the swift. Bull Mar Sci 23:260–279

    Google Scholar 

  • Lange R, Plickert G, Miller WA (1989) Histocompatibility in a low invertebrate, Hydractinia echinata: analysis of the mechanism of rejection. J Exp Zool 249:284–292

    Article  Google Scholar 

  • Leclerc M (1996) Humoral factors in marine invertebrate. In: Rinkevich B, Müller WEG (eds) Progress in molecular and subcellular biology: invertebrate immunology. Springer, Berlin Heidelberg New York, pp 1–9

    Google Scholar 

  • Lenhoff HM, Muscatine L (1963) Symbiosis: on the role of algae symbiotic with hydra Science 142:956–958

    Google Scholar 

  • Lubbock R (1980) Clone-specific cellular recognition in a sea anemone. Proc Natl Acad Sci USA 77:6667–6669

    Article  PubMed  CAS  Google Scholar 

  • Medina M, et al (2001) Evaluating hypotheses of basal animal phylogeny using complete sequences of large and small subunit rRNA. Proc Natl Acad Sci USA 98:9707–9712

    Article  PubMed  CAS  Google Scholar 

  • Meinardi E, Florin-Christensen M, Paratcha G, Azcurra JM, Florin-Christensen J (1995) The molecular basis of the self/nonself selectivity of a coelenterate toxin. Biochem Biophys Res Commun. 216:348–354

    Article  PubMed  CAS  Google Scholar 

  • Miller DJ, Ball EE, Technau U (2005) Cnidarians and ancestral genetic complexity in the animal kingdom. Trends Genet 21:536–539

    Article  PubMed  CAS  Google Scholar 

  • Miller DJ, Hemmrich G, Ball EE, Hayward DC, Khalturin K, Funayama N, Agata K, Bosch TCG (2007) The innate immune repertoire in cnidaria – ancestral complexity and stochastic gene loss. Genome Biol 8:R59

    Article  PubMed  CAS  Google Scholar 

  • Mokady O, Buss LW (1996) Transmission genetics of allorecognition in Hydractinia symbiolongicarpus (Cnidaria: Hydrozoa). Genetics 143:823–827

    PubMed  CAS  Google Scholar 

  • Müller WEG, Müller I, Zahn RK, Maidhof A (1984) Intraspecific recognition system in scleractinian corals: morphological and cytochemical description of the autolysis mechanism. J Histochem Cytochem 32:285–288

    PubMed  Google Scholar 

  • O’Brien TL (1982) Inhibition of vacuolar membrane fusion by intracellular symbiotic algae in Hydra viridis (Florida strain). J Exp Zool 223:211–218

    Article  PubMed  Google Scholar 

  • Ovchinnikova TV, Balandin SV, Aleshina GM, Tagaev AA, Leonova YF, Krasnodembsky ED, Men’shenin AV, Kokryakov VN (2006) Aurelin, a novel antimicrobial peptide from jellyfish Aurelia aurita with structural features of defensins and channel-blocking toxins. Biochem Biophys Res Commun S348:514–523

    Article  CAS  Google Scholar 

  • Phillips JH (1963) Immune mechanisms in the phylum Coelenterata. In: Dougherty EC (ed) The lower metazoan: comparative biology and phylogeny. University of California Press, Berkeley, pp 425–431

    Google Scholar 

  • Raftos DA (1996) Histocompatibility reactions in invertebrates.In: Cooper EL (ed) Invertebrate immune responses: cell activities and the environment. (Advances in comparative and environmental physiology, vol 24) Springer, Berlin Heidelberg New York, pp 77–121

    Google Scholar 

  • Richardson CA, Dustan P, Lang J (1979) Maintenance ofliving space by sweeper tentacles of Montastrea cavernosa, a Caribbean reef coral. Mar Biol 55:181–186

    Article  Google Scholar 

  • Rodriguez-Lanetty M, Phillips W, Weis VM (2006) Transcriptome analysis of a cnidarian–dinoflagellate mutualism reveals complex modulation of host gene expression. BMC Genomics 7:23

    Article  PubMed  CAS  Google Scholar 

  • Sebens KP (1984) Agonistic behavior in the intertidal sea anemone Arthropleura xanthogrammica. Biol Bull (Woods Hole, Mass) 166:457–472

    Article  Google Scholar 

  • Sebens KP, Miles JS (1988) Sweeper tentacles in a gorgoniaoctocoral: morphological modifications for interference competition. Biol Bull (Woods Hole, Mass) 175:378–387

    Article  Google Scholar 

  • Shenk MA, Buss LW (1991) Ontogenetic changes in fusibility in the colonial hydroid Hydractinia symbiolongicarpus. J Exp Zool 257:80–86

    Article  Google Scholar 

  • Technau U, et al (2005) Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. Trends Genet 21:633–639

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Wellington GM (1980) Reversal of digestive interactions between Pacific reef corals: mediation by sweeper tentacles. Oecologia 47:340–343

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Yund PO, Cunningham CW, Buss LW (1987) Recruitment and post-recruitment interactions in a colonial hydroid. Ecology 68:971–982

    Article  Google Scholar 

  • Yund PO, Parker HM (1989) Population structure of the colonial hydroid Hydractinia sp. nov. C in the Gulf of Maine. J Exp Mar Biol Ecol 125:63–82

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2008 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Bosch, T.C.G. (2008). The Path Less Explored: Innate Immune Reactions in Cnidarians. In: Heine, H. (eds) Innate Immunity of Plants, Animals, and Humans. Nucleic Acids and Molecular Biology, vol 21. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-73930-2_2

Download citation

Publish with us

Policies and ethics