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The effects of temperature and light on particles associated with crayfish visual membrane: a freeze-fracture analysis and electrophysiological study

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Summary

Depending on the pre-experimental treatment, densities as well as sizes of particles associated with the visual membranes in the eyes ofProcambarus clarkii varied. The highest mean particle density (5268 ± 969 μm2) and the smallest mean particle diameter (5.57 ± 1.35 nm) were found in crayfish which had been kept in the dark for 10 weeks in aerated fresh water of 10 ° C. Crayfish kept under a 12 h dark/light regime in water of 10 ° C or 30 ° C for three weeks displayed particle densities of 1076 ± 180 and 2899 ± 249 μm−2, respectively; particle diameters were of the order of 8 nm.

Temperature did not alter the shape or the slope of theV/logI curves, but ERG recordings show that maximum spectral sensitivity was shifted from λmax=560 nm in cold water crayfish (10 ° C) to λmax=580 nm in crayfish from the 30 ° C tank, and that the 10 ° C curve was somewhat narrower than the 30 ° C curve. It is suggested that the observed shift was caused by a combination of factors, of which the following may have played key roles: (1) The filter effect of screening pigment granules and other intracellular components such as vesicles, vacuoles, endoplasmic reticulum, and mitochondria, some of which were developed to a considerably greater extent in 30 ° C material; (2) increased membrane fluidity due to higher temperature as well as the presence of photoproducts in the light, and the ‘countermeasures’ taken by the visual pigment molecules to stabilize the lipid bilayer, e.g. higher density, possible 12-s-cis linkages etc.; and (3) increased regeneration or synthesis of rhodopsin due to higher metabolic activity of retinula cells at higher temperatures.

Temperature-induced changes of visual pigments in a variety of organisms are discussed and evidence for the rhodopsin-aggregate model of crayfish visual pigment is presented. It is concluded that the retinula cytoplasm is involved in restoring depleted stocks of photopigment, and that the biological sense of possessing an increase in red sensitivity during the warm summer months lies in the correlation of light penetration in the natural habitat ofP. clarkii and optimal exploitation of the habitat.

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References

  1. Ali, M. A. (1975) Temperature and vision.Revue Canadienne de Biologie 34, 131–86.

  2. Allen, D., Loew, E. R. &McFarland, W. M. (1982) Seasonal change in the amount of visual pigment in the retinae of fish.Canadian Journal of Zoology 60, 281–7.

  3. Arechiga, H., Fuentes-Pardo, B. &Barrera-Mera, B. (1973) Circadian rhythm of responsiveness in the visual system of the crayfish. InNeurobiology of Invertebrates (edited bySalanki, J.), pp. 403–21. Budapest: Tihany.

  4. Autrum, H. (1981) Light and dark adaptation in invertebrates. InHandbook of Sensory Physiology — Comparative Physiology and Evolution of Vision in Invertebrates, Vol. VII/6C (edited byAutrum, H.), pp. 1–91. Berlin, Heidelberg, New York: Springer Verlag.

  5. Autrum, H. &Zwehl, V. (1964) Die spektrale Empfindlichkeit einzelner Sehzellen des Bienenauges.Zeitschrift für vergleichende Physiologie 48, 357–84.

  6. Besharse, J. C. &Pfenninger, K. H. (1980) Membrane assembly in retinal photoreceptors I. Freeze-fracture analysis of cytoplasmic vesicles in relationship to disc assembly.Journal of Cell Biology 87, 451–63.

  7. Blasie, J. K. &Worthington, C. R. (1969) Planar-liquid like arrangement in photopigment molecules in frog retinal receptor disk membranes.Journal of Molecular Biology 39, 417–39.

  8. Blasie, J. K., Worthington, C. R. &Dewey, M. M. (1969) Molecular localization of frog retinal receptor photopigment by electron microscopy and low-angle X-ray diffraction.Journal of Molecular Biology 39, 407–16.

  9. Blest, A. D., Stowe, S. &Eddey, W. (1982) A labile, Ca2+-dependent cystoskeleton in rhabdomeral microvilli of blowflies.Cell and Tissue Research 223, 553–73.

  10. Bonting, S. L. &Daemen, F. J. M. (1974) Biochemistry of visual pigments in relation to visual excitation. InBiochemistry of Sensory Functions (edited byJaenicke, L.), pp. 1–22. Berlin: Springer Verlag.

  11. Boschek, B. C. &Hamdorf, K. (1976) Rhodopsin particles in the photoreceptor membrane of an insect.Zeitschrift für Naturforschung 31c, 763.

  12. Bowmaker, J. K. (1973) Spectral sensitivity and visual pigment absorbance.Vision Research 13, 783–92.

  13. Brandenburger, J. L., Eakin, R. M. &Reed, C. T. (1976) Effects of light- and dark-adaptation on the photic microvillus and photic vesicles of the pulmonate snailHelix aspersa.Vision Research 16, 1205–10.

  14. Branton, D., Bullivant, S., Gilula, N. B., Karnovsky, M. J., Moor, H., Mühlethaler, K., Northcote, D. H., Packer, L., Satir, B., Satir, P., Speth, V., Staehlin, L. A., Steere, R. L. &Weinstein, R. S. (1975) Freeze etching nomenclature.Science 190, 54–6.

  15. Brody, S. S. (1981) Temperature induced changes in the absorption spectra ofPorphyridium cruentum andAnacystis nidulans.Zeitschrift für Naturforschung 36c, 1013–20.

  16. Bruno, M. S., Barnes, S. M. &Goldsmith, T. H. (1977) The visual pigment and visual cycle of The lobsterHomarus.Journal of Comparative Physiology 120, 123–42.

  17. Changeux, J. P., Benedetti, L., Bourgeois, J. -P., Brisson, A., Cartaud, J., Devaux, P., Grünhagen, H., Moreau, M., Popot, J. -L., Sobel, A. &Weber, M. (1975) Some structural properties of the cholinergic receptor protein in its membrane environment relevant to its function as a pharmacological receptor.Cold Spring Harbor Symposium on Quantitative Biology 140, 211–320.

  18. Chen, Y. S. &Hubbell, W. L. (1973) Temperature- and light-dependent structural changes in rhodopsin lipid membranes.Experimental Eye Research 17, 517–32.

  19. Clarke, S. (1975) The size and detergent binding of membrane proteins.Journal of Biological Chemistry 250, 5459–69.

  20. Corless, J. M., Cobbs, W. H., Costello, J. M. &Robertson, J. D. (1976) On the asymmetry of frog retinal rod outer segment disk membranes.Experimental Eye Research 23, 295–324.

  21. Cossins, A. R. &Prosser, C. L. (1978) Evolutionary adaptation of membranes to temperatures.Proceedings of the National Academy of Sciences, USA 75, 2040–3.

  22. Cronin, T. W. &Goldsmith, T. H. (1982) Photosensitivity spectrum of crayfish rhodopsin measured using fluorescence of metarhodopsin.Journal of General Physiology 79, 313–32.

  23. Cummins, D. &Goldsmith, T. H. (1981) Cellular identification of the violet receptor in the crayfish eye.Journal of Comparative Physiology 142, 199–202.

  24. Czeczuga, B. (1980) Changes occurring during the annual cycle in the carotenoid content ofGammarus lacustris G.O. Sars (Crustacea: Amphipoda) specimens from the river Narew.Comparative Biochemistry and Physiology 66B, 569–72.

  25. Datz, G. &Döhler, G. (1981) Light-dependent changes in the lipid and fatty acid composition of phycocyanin-free photosynthetic lamellae ofSynechococcus.Zeitschrift für Naturforschung 36C, 856–62.

  26. Eakin, R. M. (1982) Continuity and diversity in photoreceptors. InVisual Cells in Evolution (edited byWestfall, J. A.), pp. 91–105. New York: Raven Press.

  27. Eccles, F., Tiang, K. M. &Meyer-Rochow, V. B. (1983) Electrophysiological and histological studies on the eye of the freshwater crayfishParanephrops planifrons.Zoologisches Jahrbuch für Physiologie 87, 477–89.

  28. Eguchi, E. (1965) Rhabdom structure and receptor potentials in single crayfish retinular cells.Journal of Cellular and Comparative Physiology 66, 411–29.

  29. Eguchi, E. &Waterman, T. H. (1976) Freeze-etch and histochemical evidence for cycling in crayfish photoreceptor membranes.Cell and Tissue Research 169, 419–34.

  30. Eguchi, E. &Waterman, T. H. (1979) Longterm dark-induced fine structural changes in crayfish photoreceptor membrane.Journal of Comparative Physiology 131, 191–203.

  31. Fernandez, H. R. &Nickel, E. E. (1976) Ultrastructural and molecular characteristics of crayfish photoreceptor membranes.Journal of Cell Biology 69, 721–31.

  32. Fujimoto, K., Yanase, T. &Ishizuka, I. (1966) The visual substance of the crayfishProcambarus clarkii.Memoirs of the Osaka Gakugei University B15, 109–14.

  33. Gale, J. G. &Williams, T. P. (1980) Light adaptation and temperature effects in rate PIII retinal response: Analysis with a two-state model.Proceedings of the National Academy of Sciences, USA 77, 4021–5.

  34. Gilardi, R., Karle, J., Karle, W. &Sperling, W. (1971) Crystal structure of the visual chromophores, 11-cis and all-trans retinal.Nature 232, 187–9.

  35. Goldsmith, T. H. (1965) Do flies have a red receptor?Journal of General Physiology 49, 265–87.

  36. Goldsmith, T. H. (1978) The spectral absorption of crayfish rhabdoms: pigment, photo-product, and pH-sensitivity.Vision Research 18, 463–73.

  37. Goldsmith, T. H. &Fernandez, H. R. (1968) Comparative studies of crustacean spectral sensitivity.Zeitschrift für Vergleichende Physiologie 60, 156–75.

  38. Hafner, G. S., Tokarski, T. &Hammond-Soltis, G. (1982) Development of the crayfish retina: a light and electron microscopic study.Journal of Morphology 173, 101–18.

  39. Ham, W. T., Mueller, H. A. &Sliney, D. H. (1976) Retinal sensitivity to damage from short wavelength light.Nature 260, 153–5.

  40. Ham, W. T., Ruffalo, J. J., Mueller, H. A. &Guerry, D. (1980) The nature of retinal radiation damage: dependence on wavelength, power level and exposure time.Vision Research 20, 1105–12.

  41. Hamdorf, K. (1979) The physiology of invertebrate visual pigments. InHandbook of Sensory Physiology — Vision in Invertebrates VII/6A (edited byAutrum, H.), pp. 145–224. Berlin: Springer Verlag.

  42. Hariyama, T., Yoshida, M., Eguchi, E. &Meyer-Rochow, V. B. (1982) Effect of circadian rhythm on spectral sensitivity and eye structure inLigia exotica (Isop.).Acta physiologica scandinavica Suppl.508, 37.

  43. Harri, M. &Florey, E. (1979) The effects of acclimation temperature on a neuromuscular system of the crayfishAstacus leptodactylus.Journal of Experimental Biology 78, 281–93.

  44. Harris, W. A., Ready, D. E., Lipson, E. D. &Hudspeth, A. J. (1977) Vitamin A deprivation andDrosophila photopigments.Nature 266, 648–50.

  45. Hollyfield, J. G. (1979) Membrane addition to photoreceptor outer segments: progressive reduction in the stimulatory effect of light with increased temperature.Investigative Ophthalmology and Visual Science 18, 977–81.

  46. Honig, B. (1978) Light energy transduction in visual pigments and bacteriorhodopsin.Annual Review of Physiology 29, 31–57.

  47. Horridge, G. A., Marcelja, L., Jahnke, R. &Matic, T. (1983) Single electrode studies on the retina of the butterflyPapilio.Journal of Comparative Physiology 150, 271–94.

  48. Jähnig, F. (1981) Critical effects from lipid-protein interaction in membranes II. Interpretation of experimental results.Biophysics Journal 36, 347–57.

  49. Jan, L. Y. &Revel, J. -P. (1974) Ultrastructural localization of rhodopsin in the vertebrate retina.Journal of Cell Biology 62, 257–73.

  50. Kennedy, D. &Bruno, M. S. (1961) The spectral sensitivity of crayfish and lobster vision.Journal of General Physiology 44, 1089–102.

  51. Key, K. H. L. &Day, M. F. (1954) A temperature-controlled physiological colour response in the grasshopperKosciuscola tristis Sjöstr. (Orthoptera; Acridiae).Australian Journal of Zoology 2, 309–39.

  52. Kirschfeld, K. (1982) Carotenoid pigments: their possible role in protecting against photooxidation in eyes and photoreceptor cells.Proceedings of the Royal Society of London, Series B 216, 71–85.

  53. Kivivuori, L. (1982) Temperature acclimation of the caudal photoreceptor response in the crayfishAstacus astacus L.Comparative Biochemistry and Physiology 72A, 17–21.

  54. Kleinholz, L. H. (1966) Hormonal regulation of retinal pigment migration in crustaceans. InThe functional Organisation of the Compound Eye (edited byBernhard, C. G.), pp. 89–101. Oxford: Pergamon.

  55. Kong, K. L. &Goldsmith, T. H. (1977) Photosensitivity of retinular cells in white-eyed crayfish (Procambarus clarkii).Journal of Comparative Physiology 122, 273–88.

  56. Larrivee, D. &Goldsmith, T. H. (1982) Spectral dimorphism of crayfish visual pigment in solution.Vision Research 22, 727–37.

  57. Levine, J. S. &Macnichol, E. G. (1982) Colour vision in fishes.Scientific American 246, 140–9.

  58. Lewis, J. W., Winterle, J. S., Powers, M. A., Kliger, D. S. &Dratz, E. A. (1981) Kinetics of rhodopsin photolysis intermediates in retinal rod disk membranes — I. Temperature dependence of lumirhodopsin and metarhodopsin-I kinetics.Photochemistry and Photobiology 34, 375–84.

  59. Macdonald, J. A. (1981) Temperature compensation in the peripheral nervous system: Antarctic versus temperate poikilotherms.Journal of Comparative Physiology 142, 411–18.

  60. McFarland, W. N. &Allen, D. M. (1977) The effect of extrinsic factors on two distinctive rhodopsin-porphyropsin systems.Canadian Journal of Zoology 55, 1000–9.

  61. Meng, M. S., West, G. C. &Irving, L. (1969) Fatty acid composition of caribou bone marrow.Comparative Biochemistry and Physiology 30, 187–91.

  62. Meyer-Rochow, V. B. (1978) The eyes of mesopelagic crustaceans IIStreetsia challengeri (Amphipoda).Cell and Tissue Research 186, 337–46.

  63. Meyer-Rochow, V. B. (1982) The divided eye of the isopodGlyptonotus antarcticus: effects of unilateral dark adaptation and temperature elevation.Proceedings of the Royal Society of London, Series B 215, 433–50.

  64. Meyer-Rochow, V. B. &Eguchi, E. (1983) Ultrastructure du rhabdome deProcambarus clarkii immédiatement et vingt heures aprés l'exposition à la lumière ultraviolette (350 nm) et verte (580 nm) d'un contenu photonique égal.Biology of the Cell 48, 185–90.

  65. Meyer-Rochow, V. B. &Horridge, G. A. (1975) The eye ofAnoplognathus (Coleoptera, Scarabaeidae).Proceedings of the Royal Society of London, Series B 188, 1–30.

  66. Meyer-Rochow, V. B. &Pyle, C. (1980) Fatty acid analysis of lens and retina of two Antarctic fishes and of the head and body of the Antarctic amphipodOrchomene plebs.Comparative Biochemistry and Physiology 65B, 395–8.

  67. Meyer-Rochow, V. B. &Tiang, K. M. (1979) The effects of light and temperature on the structural organization of the eye of the Antarctic amphipodOrchomene plebs (Crustacea).Proceedings of the Royal Society of London, Series B 206, 353–68.

  68. Meyer-Rochow, V. B. &Tiang, K. M. (1982) Comparison between temperature-induced changes and effects caused by dark/light adaptation in the eyes of two species of Antarctic crustaceans.Cell and Tissue Research 221, 625–32.

  69. Meyer-Rochow, V. B. &Tiang, K. M. (1984) The eye ofJasus edwardsii (Crustacea, Decapoda, Palinuridae): electrophysiology, histology, and behaviour.Zoologica 45, 1–685.

  70. Miller, W. H. (1979) Ocular optical filtering. InHandbook of Sensory Physiology Vol. VII/6A (edited byAutrum, H.), pp. 70–143. Berlin: Springer Verlag.

  71. Munz, F. W. &McFarland, W. N. (1977) Evolutionary adaptations of fishes to the photic environment. InHandbook of Sensory Physiology Vol. VII/5 (edited byCrescitelli, F.), pp. 193–274. Berlin: Springer Verlag.

  72. Nagy, A. R. &Witkovsky, P. (1981) A freeze-fracture study of synaptogenesis in the distal retina of larvalXenopus.Journal of Neurocytology 10, 897–919.

  73. Nickel, E. E. &Menzel, R. (1976) Insect UV- and green-photoreceptor membranes studied by the freeze-fracture technique.Cell and Tissue Research 175, 357–68.

  74. Nosaki, H. (1969) Electrophysiological study of colour encoding in the compound eye of crayfish,Procambarus clarkii.Zeitschrift für vergleichende Physiologie 64, 318–23.

  75. Nozawa, Y., Iida, H., Fukushima, H., Ohki, K. &Ohnishi, S. (1974) Studies onTetrahymena membranes: temperature induced alterations in fatty acid composition of various membrane fractions.Biochimica et Biophysica Acta 367, 134–47.

  76. Ostroy, S. E. (1978) Characteristics ofDrosophila rhodopsin in wildtype andnorp A-vision transduction mutants.Journal of General Physiology 72, 717–32.

  77. Perrelet, A., Bauer, H. &Fryder, V. (1972) Fracture faces of an insect rhabdome.Journal de Microscopie 13, 97–106.

  78. Peters, R. (1981) Translation diffusion in the plasma membrane of single cells as studied by fluorescence microphotolysis.Cell Biology International Reports 5, 733–60.

  79. Razmjoo, S. &Hamdorf, K. (1976) Visual sensitivity and the variation of total photopigment content in the blowfly photoreceptor membrane.Journal of Comparative Physiology 105, 279–86.

  80. Rutherford, D. J. &Horridge, G. A. (1965) The rhabdom of the lobster eye.Quarterly Journal of Microscopical Science 106, 119–30.

  81. Sjöstrand, F. S., Kreman, M. &Crescitelli, F. (1979) Freeze-fracture analysis of photoreceptor cell outer segment disks after minimal extraction of rhodopsin.Journal of Ultrastructure Research 69, 53–67.

  82. Sinensky, M. (1974) Homeoviscous adaptation — a homeostatic process that regulates the viscosity of membrane lipids inEscherichia coli.Proceedings of the National Academy of Sciences, USA 71, 522–5.

  83. Singer, S. J. (1975) Architecture and topography of biologic membranes. InCell Membranes, Biochemistry, Cell Biology and Pathology (edited byWeisman, G. andClaiborne, R.), pp. 35–44. New York: HP Publishing Corporation.

  84. Singer, S. J. &Nicholson, G. L. (1972) The fluid mosaic model of the structure of the cell membranes.Science 175, 720–31.

  85. Srinivasan, M. V., Bernard, G. D. &Stavenga, D. G. (1977) Effects of temperature on the pupillary response of the butterfly eye.Biological Bulletin 153, 445–6.

  86. Stieve, H. (1963) Das Belichtungspotential der Retina des Einsiedlerkrebses in Abhängigkeit von der Temperatur.Zeitschrift für vergleichende Physiologk 46, 249–75.

  87. Stieve, H. (1981) Roles of calcium in visual transduction in vertebrates. InSense Organs (edited byLaverack, M. S. andCosens, D. J.), pp. 163–85. London: Blackie.

  88. Stowe, S. (1980) Rapid synthesis of photoreceptor membrane and assembly of new microvilli in a crab at dusk.Cell and Tissue Research 211, 419–40.

  89. Suzuki, T., Makino-Tasaka, M. &Eguchi, E. (1984) 3-dehdroretinal (Vitamin A2 aldehyde) in crayfish eye.Vision Research (in press).

  90. Szabo, G. &Waldbillig, R. C. (1982) Lipid model membranes.Methods in Experimental Physics 20, 513–43.

  91. Tschugunoff, V. N. (1913) Über die Veränderung des Auges beiLeptodora kindtii (Focke) unter dem Einfluss von Nahrungsentziehung.Biologisches Centralblatt 33, 351–61.

  92. Tsin, A. T. &Beatty, D. D. (1977) Visual pigment changes in rainbow trout in response to temperature.Science 195, 1358–9.

  93. Usukura, J. &Yamada, E. (1981) Molecular organisation of the rod outer segment: a deep-etching study with rapid freezing using unfixed frog retina.Biomedical Research 2, 177–93.

  94. Veron, J. E. N. (1976) Response of Odonata chromatophores to environmental stimuli.Journal of Insect Physiology 22, 19–30.

  95. Vogt, K. (1983) Is the fly visual pigment a rhodopsin?Zeitschrift für Naturforschung 38c, 329–33.

  96. Wald, G. (1967) Visual pigments of crayfish.Nature 215, 1131–3.

  97. Wald, G. (1973) Visual pigments and photoreceptor physiology. InBiochemistry and Physiology of Visual Pigments (edited byLanger, H.), pp. 1–13. Berlin: Springer Verlag.

  98. Woodcock, A. E. R. &Goldsmith, T. H. (1970) Spectral responses of sustaining fibres in the optic tracts of crayfishProcambarus.Zeitschrift für vergleichende Physiologie 69, 117–33.

  99. Yamada, E. (1979) Electron microscopy of photoreceptive membranes.Journal of Electron Microscopy 28, Suppl. S79-S86.

  100. Yamamoto, T. Y., Tonosaki, A. &Watanabe, H. (1974) Complementary faces of the rod disc membrane in freeze-fracture replicas.Tohoku Journal of Experimental Medicine 113, 313–17.

  101. Yoshizawa, T. &Wald, G. (1963) Pre-lumirhodopsin and the bleaching of visual pigments.Nature 197, 1279–86.

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Meyer-Rochow, V.B., Eguchi, E. The effects of temperature and light on particles associated with crayfish visual membrane: a freeze-fracture analysis and electrophysiological study. J Neurocytol 13, 935–959 (1984). https://doi.org/10.1007/BF01148595

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Keywords

  • Lipid
  • Fresh Water
  • Particle Diameter
  • Cold Water
  • Natural Habitat