On the three visual pigments in the retina of the firefly squid, Watasenia scintillans

Summary

The deep-sea bioluminescent squid, Watasenia scintillans, has three visual pigments: The major one (A1 pigment) is based on retinal and has λ max = 484 nm, the second one (A2 pigment) is based on 3-dehydroretinal and has λ max = 500 nm, and the third one (A4 pigment) is based on 4-hydroxyretinal and has λ max = 470 nm. The distribution of these 3 visual pigments in the retina was studied by HPLC analysis of the retinals in retina slices obtained by microdissection. It was found that A1 pigment was not located in the specific region of the ventral retina receiving the down-welling light which contains very long photoreceptor cells, forming two strata. A2 and A4 pigment were found exclusively in the proximal pinkish stratum and in the distal yellowish stratum. The role of these pigments in the retina is hypothesized to involve spectral discrimination. The extraction and analysis of retinoids to determine the origin of 3-dehydroretinal and 4-hydroxyretinal in the mature squid showed only a trace amount of 4-hydroxyretinol in the eggs. Similar analysis of other cephalopods collected near Japan showed the absence of A2 or A4 pigment in their eyes.

This is a preview of subscription content, access via your institution.

Abbreviations

HPLC :

high-performance liquid chromatography

IS :

inner segment

OS :

outer segment

References

  1. Bridges CDB (1972) The rhodopsin-porphyropsin visual system. In: Dartnall HJA (ed) Handbook of sensory physiology, VII/1. Springer, Berlin Heidelberg New York, pp 417–480

    Google Scholar 

  2. Bridges CDB, Alvarez RA (1980) Measurement of the vitamin A cycle. Methods Enzymol 81:463–485

    Google Scholar 

  3. Dartnall HJA (1975) Assessing the fitness of visual pigments for their photic environments. In: Ali MA (ed) Vision in fishes. Plenum Press, New York London, pp 543–563

    Google Scholar 

  4. Denton EJ, Gilpin-Brown JB, Wright PG (1970) On the filters in the photophores of mesopelagic fish and on a fish emitting red light and especially sensitive to red light. J Physiol 208:72P-73P

    Google Scholar 

  5. Denton EJ, Locket NA (1989) Possible wavelength discrimination by multibank retinae in deep-sea fishes. J Mar Biol Assoc UK 69:409–435

    Google Scholar 

  6. Eakin RM (1972) Structure of invertebrate photoreceptors. In: Dartnall HJA (ed) Handbook of sensory physiology, VII/1. Springer, Berlin Heidelberg New York, pp 626–684

    Google Scholar 

  7. Groenendijk GWT, Grip WJ de, Daemen FJM (1980) Quantitative determination of retinals with complete retention of their geometric configuration. Biochim Biophys Acta 617:430–438

    Google Scholar 

  8. Kampa E (1970) Underwater daylight and moonlight measurements in the eastern North Atlantic. J Mar Biol Assoc UK 50:397–420

    Google Scholar 

  9. Kito Y, Nashima K, Sugahara M (1979) Photoreceptor membranes. In: Sibatani K (ed) Biological and chemical utilization of solar energy. Gakkai Press, Tokyo, pp 80–95 (in Japanese)

    Google Scholar 

  10. Kito Y, Seki T, Suzuki T, Uchiyama I (1986) 3-Dehydroretinal in the eye of a bioluminescent squid, Watasenia scintillans. Vision Res 26:275–279

    Google Scholar 

  11. Locket NA (1977) Adaptations to the deep-sea environment. In: Crescitelli F (ed) Handbook of sensory physiology, vol VII/3. The visual system in vertebrates. Springer, Berlin Heidelberg New York, pp 67–192

    Google Scholar 

  12. Lythgoe JN (1980) Vision of fish: ecological adaptations. In: Ali MA (ed) Environmental physiology of fishes. Plenum Publishing Corp, New York, pp 68–73

    Google Scholar 

  13. Makino M, Nagai K, Suzuki T (1983) Seasonal variation of the vitamin A-based visual pigment in the retina of adult bullfrog, Rana catesbeiana. Vision Res 23:199–204

    Google Scholar 

  14. Masuda H, Michinomae M, Seidou M, Kito Y (1988) Light and electron microscopic investigation of cellular architecture in the retina of the firefly squid, Watasenia scintillans. Zool Sci 5:1201

    Google Scholar 

  15. Matsui S, Seidou M, Horiuchi S, Uchiyama I, Kito Y (1988a) Adaptation of a deep-sea cephalopod to the photic environment. J Gen Physiol 92:55–66

    Google Scholar 

  16. Matsui S, Seidou M, Uchiyama I, Sekiya N, Hiraki K, Yoshihara K, Kito Y (1988b) 4-Hydroxyretinal, a new visual pigment chromophore found in the bioluminescent squid, Watasenia scintillans. Biochim Biophys Acta 966:370–374

    Google Scholar 

  17. Munz FW, McFarland WN (1977) Evolutionary adaptations of fishes to the photic environment. In: Crescitelli F (ed) Handbook of sensory physiology, vol VII/4. The visual system in vertebrates. Springer, Berlin Heidelberg New York, pp 193–274

    Google Scholar 

  18. Nashima K, Mitsudo M, Kito Y (1979) Molecular weight and structural studies on cephalopod rhodopsin. Biochem Biophys Acta 579:155–168

    Google Scholar 

  19. Pappin DJC, Findlay JBC (1984) Sequence variability in the retinal-attachment domain of mammalian rhodopsins. Biochem J 217:605–613

    Google Scholar 

  20. Partridge JC, Archer SN, Lythgoe JN (1988) Visual pigments in the individual rods of deep-sea fishes. J Comp Physiol A 162:543–550

    Google Scholar 

  21. Renk G, Grover T, Crouch R, Mao B, Ebrey TG (1981) A spin labeled retinal pigment analogue of the purple membrane. Photochem Photobiol 33:489–494

    Google Scholar 

  22. Seidou M, Kubota I, Hiraki K, Kito Y (1988) Amino acid sequence of the retinal binding site of squid visual pigment. Biochem Biophys Acta 957:318–321

    Google Scholar 

  23. Suzuki T, Makino-Tasaka M (1983) Analysis of retinal and 3-dehydroretinal in the retina by HPLC. Anal Biochem 29:111–119

    Google Scholar 

  24. Yuuki Y (1985) Spawning and growth of Watasenia scintillans in the southwestern Japan Sea. Report Shimane Prefec Fish Exp Station 49:1–6 (in Japanese)

    Google Scholar 

Download references

Author information

Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Seidou, M., Sugahara, M., Uchiyama, H. et al. On the three visual pigments in the retina of the firefly squid, Watasenia scintillans . J Comp Physiol A 166, 769–773 (1990). https://doi.org/10.1007/BF00187321

Download citation

Key words

  • 3-dehydroretinal
  • 4-hydroxyretinal
  • Bioluminescence
  • Squid visual pigment
  • Retinal