Skip to main content
Log in

Mechanosensitivity in the model sea anemone Nematostella vectensis

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Tentacles of the sea anemone, Nematostella vectensis, are covered with hair bundles. Hair bundles were deflected by water jets to test whether they are mechanoreceptors. Electrophysiological recordings confirm that deflections of hair bundles induce transients in membrane current. In a different species of anemone, hair bundle mechanoreceptors are known to change shape and responsiveness according to the activity of chemoreceptors that bind prey-derived compounds including N-acetylated sugars. In Nematostella, hair bundles significantly elongate upon exposure to NANA, an N-acetylated sugar. Based on a bioassay in which discharged nematocysts are counted in gelatin-coated test probes touched to tentacles, we find that NANA shifts vibration dependent discharge of basitrich nematocysts to lower frequencies overlapping those produced during swimming by known prey including planktonic crustaceans. Furthermore, we find for the first time that vibration detection extends at least 2.5 cm beyond the tentacle tips. Thus, Nematostella likely employs its hair bundles to detect swimming movements of nearby prey.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ashmore JF (1991) The electrophysiology of hair cells. Annu Rev Physiol 53:465–476

    Article  PubMed  CAS  Google Scholar 

  • Bleckmann H, Topp G (1981) Surface wave sensitivity of the lateral line organs of the topminnow Aplocheilus lineatus. Naturwissenschaften 68:624–625

    Article  Google Scholar 

  • Bolz H, von Brederlow B, Ramirez A, Bryda EC, Kutsche K, Nothwang HG, Seeliger M, Cabrera M, Vila MC, Molina OP (2001) Mutation of CDH23, encoding a new member of the cadherin gene family, causes Usher syndrome type 1D. Nat Genet 27:108–112

    Article  PubMed  CAS  Google Scholar 

  • Bork JM, Peters LM, Riazuddin S, Bernstein SL, Ahmed ZM, Ness SL, Polomeno R, Ramesh A, Schloss M, Srisailpathy CR (2001) Usher syndrome 1D and nonsyndromic autosomal recessive deafness DFNB12 are caused by allelic mutations of the novel cadherin-like gene CDH23. Am J Hum Genet 68:26–37

    Article  PubMed  CAS  Google Scholar 

  • Budelmann BU, Bleckmann H (1988) A lateral line analogue in cephalopods: water waves generate generate microphonic potentials in the epidermal head lines of Sepia and Lolliguncula. J Comp Physiol A 163:1–5

    Article  Google Scholar 

  • Darling JA, Reitzel AR, Burton PM, Mazza ME, Ryan JF, Sullivan JC, Finnerty JR (2005) Rising starlet: the starlet sea anemone, Nematostella vectensis. Bioessays 27:211–221

    Article  PubMed  CAS  Google Scholar 

  • Di Palma F, Holme RH, Bryda EC, Belyantseva IA, Pellegrino R, Kachar B, Steel KP, Noben-Trauth K (2001) Mutations in Cdh23, encoding a new type of cadherin, cause stereocilia disorganization in waltzer, the mouse model for Usher syndrome type 1D. Nat Genet 27:103–107

    Article  PubMed  CAS  Google Scholar 

  • Gallager SM (1993) Hydrodynamic disturbances produced by small zooplankton: case study for the veliger larva of a bivalve mollusk. J Plankton Res 15:1277–1296

    Article  Google Scholar 

  • Hand C, Uhlinger KR (1992) The culture, sexual and asexual reproduction, and growth of the sea anemone Nematostella vectensis. Biol Bull 182:169–176

    Article  Google Scholar 

  • Hand C, Uhlinger KR (1994) The unique, widely distributed, estuarine sea anemone Nematostella vectensis Stephenson: a review, new facts and questions. Estuaries 17:508–510

    Article  Google Scholar 

  • Howard J, Roberts WM, Hudspeth AJ (1988) Mechanoelectrical transduction by hair cells. Annu Rev Biophys Chem 17:99–124

    Article  CAS  Google Scholar 

  • Hudspeth AJ (1985) The cellular basis of hearing: the biophysics of hair cells. Science 230:745–752

    Article  PubMed  CAS  Google Scholar 

  • Hudspeth AJ (1997) How hearing happens. Neuron 19:947–950

    Article  PubMed  CAS  Google Scholar 

  • Kachar B (1985) Asymmetric illumination contrast: a method of image formation for video light microscopy. Science 227:766–768

    Article  PubMed  CAS  Google Scholar 

  • LeMasurier M, Gillespie PG (2005) Hair-cell mechanotransduction and cochlear amplification. Neuron 48:403–415

    Article  PubMed  CAS  Google Scholar 

  • Mariscal RN (1974) Nematocysts. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology reviews and new perspectives. Academic, New York, pp 129–178

    Google Scholar 

  • Martindale MQ, Pang K, Finnerty JR (2004) Investigating the origins of triploblasty: ‘mesodermal’ gene expression in a diploblastic animal, the sea anemone Nematostella vectensis (phylum, Cnidaria; class, Anthozoa). Development 131:2463–2474

    Article  PubMed  CAS  Google Scholar 

  • Matus DQ, Pang K, Daly M, Martindale MQ (2007) Expression of Pax gene family members in the antozoan cnidarian, Nematostella vectensis. Evol Dev 9:25–38

    PubMed  CAS  Google Scholar 

  • Mire P, Nasse J (2002) Hair bundle motility induced by chemoreceptors in anemones. Hear Res 163:111–120

    Article  PubMed  CAS  Google Scholar 

  • Mire P, Watson GM (1997) Mechanotransduction of hair bundles arising from multicellular complexes in anemones. Hear Res 113:224–234

    Article  PubMed  CAS  Google Scholar 

  • Mire-Thibodeaux P, Watson GM (1994) Morphodynamic hair bundles arising from sensory cell/supporting cell complexes frequency-tune nematocyst discharge in sea anemones. J Exp Zool 268:281–292

    Article  Google Scholar 

  • Montgomery JC, MacDonald JA (1987) Sensory tuning of the lateral line receptors in Antartic fish to the movements of planktonic prey. Science 235:195–196

    Article  PubMed  Google Scholar 

  • Nicolson T, Rusch A, Friedrich RW, Granato M, Ruppersberg JP, Nüsslein-Volhand C (1998) Genetic analysis of vertebrate sensory hair cell mechanosensation: the zebrafish circler mutants. Neuron 20:271–283

    Article  PubMed  CAS  Google Scholar 

  • Sebens KP (1998 Marine flora and fauna of the Eastern United States. Anthozoa: Actiniaria, Corallimorpharia, Ceriantharia and Zoanthidea. N.O.A.A. Technical Rpt. NMFS. 141. 68 pp

  • Siemens J, Lillo C, Dumont RA, Reynolds A, Williams DS, Gillespie PG, Muller U (2004) Cadherin 23 is a component of the tip link in hair-cell stereocilia. Nature 428:950–955

    Article  PubMed  CAS  Google Scholar 

  • Sollner C, Rauch GJ, Siemens J, Geisler R, Schuster SC, Muller U, Nicolson T, Tubingen 2000 Screening Consortium (2004) Mutations in cadherin 23 affect tip links in zebrafish sensory hair cells. Nature 428:955–959

    Article  PubMed  Google Scholar 

  • Sullivan JC, Ryan JF, Watson JA, Webb J, Mullikan JC, Rokhsar D, Finnerty JR (2006) Stellabase: the Nematostella vectensis genomics database. Nucleic Acids Res 34:D495–D499

    Article  PubMed  CAS  Google Scholar 

  • Tautz J, Sandeman DC (1980) The detection of waterborne vibration by sensory hairs on the chelae of the crayfish. J Exp Biol 88:351–356

    Google Scholar 

  • Watson GM, Hessinger DA (1989) Cnidocyte mechanoreceptors are tuned to the movements of swimming prey by chemoreceptors. Science 243:1589–1591

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Mariscal RN (1983) Comparative ultrastructure of catch tentacles and feeding tentacles in the sea anemone Haliplanella. Tissue Cell 15:939–953

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Mire P (2004) Dynamic tuning of hair bundle mechanoreceptors in a sea anemone during predation. Hydrobiologica 530(531):123–128

    Article  Google Scholar 

  • Watson GM, Roberts J (1995) Chemoreceptor-mediated polymerization and depolymerization of actin in hair bundles of sea anemones. Cell Motil Cytoskel 30:208–220

    Article  CAS  Google Scholar 

  • Watson GM, Mire P, Hudson RR (1997) Hair bundles of sea anemones as a model system for vertebrate hair bundles. Hear Res 107:53–66

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Mire P, Hudson RR (1998) Frequency specificity of vibration dependent discharge of nematocysts in sea anemones. J Exp Zool 281:582–593

    Article  PubMed  CAS  Google Scholar 

  • Watson GM, Pham L, Graugnard EM, Mire P (2008) Cadherin 23-like polypeptide in hair bundle mechanoreceptors of sea anemones. J Comp Physiol A 194:811–820

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We appreciate financial support from the National Science Foundation of the United States (NSF IOB0542574). We appreciate critical comments by two anonymous reviewers and J. Malcolm Shick.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Glen M. Watson.

Additional information

Communicated by U. Sommer.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Watson, G.M., Mire, P. & Kinler, K.M. Mechanosensitivity in the model sea anemone Nematostella vectensis . Mar Biol 156, 2129–2137 (2009). https://doi.org/10.1007/s00227-009-1243-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-009-1243-9

Keywords

Navigation