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Immunohistochemical evidence for multiple photosystems in box jellyfish

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Abstract

Cubomedusae (box jellyfish) possess a remarkable visual system with 24 eyes distributed in four sensory structures termed rhopalia. Each rhopalium is equipped with six eyes: two pairs of pigment cup eyes and two unpaired lens eyes. Each eye type probably captures specific features of the visual environment. To investigate whether multiple types of photoreceptor cells are present in the rhopalium, and whether the different eye types possess different types of photoreceptors, we have used immunohistochemistry with a range of vertebrate opsin antibodies to label the photoreceptors, and electroretinograms (ERG) to determine their spectral sensitivity. All photoreceptor cells of the two lens eyes of the box jellyfish Tripedalia cystophora and Carybdea marsupialis displayed immunoreactivity for an antibody directed against the zebrafish ultraviolet (UV) opsin, but not against any of eight other rhodopsin or cone opsin antibodies tested. In neither of the two species were the pigment cup eyes immunoreactive for any of the opsin antibodies. ERG analysis of the Carybdea lower lens eyes demonstrated a single spectral sensitivity maximum at 485 nm suggesting the presence of a single opsin type. Our data demonstrate that the lens eyes of box jellyfish utilize a single opsin and are thus color-blind, and that there is probably a different photopigment in the pigment cup eyes. The results support our hypothesis that the lens eyes and the pigment cup eyes of box jellyfish are involved in different and specific visual tasks.

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References

  • Coates MM, Garm A, Theobald JC, Thompson SH, Nilsson D-E (2006) The spectral sensitivity of the lens eyes of a box jellyfish, Tripedalia cystophora (Conant). J Exp Biol 209:3758–3765

    Article  PubMed  Google Scholar 

  • de Couet HG, Tanimura T (1987) Monoclonal antibodies provide evidence that rhodopsin in the outer rhabdomeres of Drosophila melanogaster is not glycosylated. Eur J Cell Biol 44:50–66

    Google Scholar 

  • Foster RG, Garzia-Fernandez JM, Provencio I, DeGrip WJ (1993) Opsin localization and chromophore retinoids identified within the basal brain of the lizard Anolis carolinensis. J Comp Physiol [A] 172:33–45

    Article  Google Scholar 

  • Garm A, Coates MM, Gad R, Seymour J, Nilsson D-E (2007a) The lens eyes of the box jellyfish Tripedalia cystophora and Chiropsalmus sp. are slow and color-blind. J Comp Physiol [A] 193:547–557

    Article  CAS  Google Scholar 

  • Garm A, O’Connor M, Parkefelt L, Nilsson D-E (2007b) Visually guided obstacle avoidance in the box jellyfish Tripedalia cystophora and Chiropsella bronzie. J Exp Biol 210:3616–3623

    Article  PubMed  CAS  Google Scholar 

  • Garm A, Andersson F, Nilsson D-E (2008) Unique structure and optics of the lesser eyes of the box jellyfish Tripedalia cystophora. Vision Res, in press

  • Govardovskii VI, Fyhrquist N, Reuter T, Kuzmin DG, Donner K (2000) In search of the visual pigment template. Vis Neurosci 17:509–528

    Article  PubMed  CAS  Google Scholar 

  • Janssen JJM (1991) The rod visual pigment rhodopsin: in vitro expression and site specific mutagenesis. PhD Thesis, University of Nijmegen, The Netherlands

  • Land MF, Nilsson D-E (2006) General-purpose and special-purpose visual systems. In: Warrant EJ, Nilsson D-E (eds) Invertebrate vision. Cambridge University Press, Cambridge, pp 167–210

    Google Scholar 

  • Laska G, Hündgen M (1982) Morphologie und Ultrastruktur der Lichtsinnesorgane von Tripedalia cystophora Conant (Cnidaria, Cubozoa). Zool Jb Anat 108:107–123

    Google Scholar 

  • Martin VJ (2004) Photoreceptors of cubozoan jellyfish. Hydrobiologia 530/531:135–144

    Article  CAS  Google Scholar 

  • Nilsson D-E, Coates M, Gislén L, Skogh C, Garm A (2005) Advanced optics in a jellyfish eye. Nature 435:201–205

    Article  PubMed  CAS  Google Scholar 

  • Plachetzki DC, Degnan BM, Oakley TH (2007) The origins of novel protein interactions during animal opsin evolution. PLoS ONE 2:e1054

    Article  PubMed  Google Scholar 

  • Santillo S, Orlando P, De Petrocellis L, Cristino L, Guglielmotti V, Musio C (2006) Evolving visual pigments: hints from the opsin-based proteins in a phylogenetically old “eyeless” invertebrate. BioSystems 86:3–17

    Article  PubMed  CAS  Google Scholar 

  • Satterlie RA (1979) Central control of swimming in the cubomedusan jellyfish Carybdea rastonii. J Comp Physiol 133:257–267

    Article  Google Scholar 

  • Satterlie RA (2002) Neuronal control of swimming in jellyfish: a comparative story. Can J Zool 80:1654–1669

    Article  Google Scholar 

  • Schalken JJ (1987) The visual pigment rhodopsin: immunohistochemical aspects and induction of experimental autoimmune uveoretinitis. PhD Thesis, University of Nijmegen, The Netherlands

  • Skogh C, Garm A, Nilsson D-E, Ekström P (2006) The bilaterally symmetric rhopalial nervous system of box jellyfish. J Morphol 267:1391–1405

    Article  PubMed  CAS  Google Scholar 

  • Suga H, Schmid V, Gehring WJ (2008) Evolution and functional diversity of jellyfish opsins. Curr Biol 18:51–55

    Article  PubMed  CAS  Google Scholar 

  • Szél A, Tákacs L, Monistori E, Diamantstein T, Vigh-Teichmann I, Röhlich P (1986) Monoclonal antibody recognizing cone visual pigment. Exp Eye Res 43:871–883

    Article  PubMed  Google Scholar 

  • Vihtelic TS, Doro CJ, Hyde DR (1999) Cloning and characterization of six zebrafish photoreceptor opsin cDNAs and immunolocalization of their corresponding proteins. Vis Neurosci 16:571–585

    Article  PubMed  CAS  Google Scholar 

  • Weber C (1982a) Electrical activities of a type of electroretinogram recorded from the ocellus of a jellyfish, Polyorchis penicillatus (Hydromedusae). J Exp Zool 223:231–243

    Article  PubMed  CAS  Google Scholar 

  • Weber C (1982b) Electrical activity in response to light of the ocellus of the hydromedusan, Sarsia tubulosa. Biol Bull 162:413–422

    Article  Google Scholar 

  • Yamasu T, Yoshida M (1976) Fine structure of the complex ocelli of a cubomedusan, Tamoya bursaria Haeckel. Cell Tissue Res 170:325–339

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Eva Landgren, Carina Rasmussen, and Rita Wallén for expert technical assistance. This study was supported by the Swedish Research Council (D.-E. Nilsson, #621-2005-2909) and the Carlsberg Foundation (A. Garm; #2005-1-74).

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Correspondence to Peter Ekström.

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Ekström, P., Garm, A., Pålsson, J. et al. Immunohistochemical evidence for multiple photosystems in box jellyfish. Cell Tissue Res 333, 115–124 (2008). https://doi.org/10.1007/s00441-008-0614-8

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