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Coupling between action potential and bioluminescence inNoctiluca: Effects of inorganic ions and pH in vacuolar sap

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Summary

  1. 1.

    The ionic dependency of the flash-triggering action potential (FTP) evoked across the vacuolar membrane inNoctiluca was studied by injecting various salt and pH buffer solutions into the vacuole.

  2. 2.

    Electron microscopic observations showed that the peripheral cytoplasmic compartment sandwiched between vacuole and pellicle is 0.11±0.07 μm in thickness, so that it has a very small volume (Figs. 2 and 15).

  3. 3.

    The resting membrane resistance and capacitance measured across the cell surface were about 10 KΩ·cm2 and 0.8 μF/cm2, respectively. Under normal conditions the FTP, which is 50∼60 mV in amplitude, arises from a potential of −150 to −160 mV.

  4. 4.

    More than a tenfold increase in the concentration of K+, Ca2+, Mg2+, NH +4 , or SO 2−4 in the vacuole produced no significant change in the amplitude of FTP (Figs. 4 and 5).

  5. 5.

    Injections of HCl-glycine buffer solutions of various pH were used to alter the intrinsic vacuolar pH (about 3.5) within the range of 2.5 to 3.7 without damaging the cells. The FTP amplitude rose about 58 mV per unit drop in pH (Figs. 6–9, Table 1).

  6. 6.

    Crude aqueous extracts from the cells emitted light most effectively when the pH was lowered from 8.2 to 5.5. None of the other major cations found in the vacuole showed any effect on the light emission of the extract (Figs. 12 and 13).

  7. 7.

    From these findings, we propose a proton hypothesis explaining the coupling between the bioluminescence and the action potential.

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Abbreviations

FTP :

flash-triggering action potential

TRP :

tentacle regulating potential

PVC :

perivacuolar cytoplasm

TTX :

tetrodotoxin

References

  • Chang, J.J.: Electrophysiological studies of a nonluminescent form of the dinoflagellateNoctiluca miliaris. J. Cell. Comp. Physiol. 56, 33–42 (1960)

    Google Scholar 

  • DeSa, R., Hastings, J.W.: The characterization of scintillons. Bioluminescent particles from the marine dinoflagellate,Gonyaulax polyedra. J. Gen. Physiol.51, 105–122 (1968)

    Google Scholar 

  • DeSa, R., Hastings, J.W., Vatter, A.E.: Luminescent “crystalline” particles: An organized subcellular bioluminescent system. Science141, 1269–1270 (1963)

    Google Scholar 

  • Eckert, R.: Bioelectric control of bioluminescence in the dinoflagellateNoctiluca. Science147, 1140–1145 (1965)

    Google Scholar 

  • Eckert, R.: Bioelectric control of ciliary activity. Science176, 473–481 (1972)

    Google Scholar 

  • Eckert, R., Reynolds, G.T.: The subcellular origin of bioluminescence inNoctiluca miliaris. J. Gen. Physiol.50, 1429–1458 (1967)

    Google Scholar 

  • Eckert, R., Sibaoka, T.: Bioelectric regulation of tentacle movement in a dinoflagellate. J. Exp. Biol.47, 433–446 (1967)

    Google Scholar 

  • Eckert, R., Sibaoka, T.: The flash-triggering action potential of the luminescent dinoflagellateNoctiluca. J. Gen. Physiol.52, 258–282 (1968)

    Google Scholar 

  • Eckert, R., Naitoh, Y., Machemer, H.: Calcium in the bioelectric and motor functions ofParamecium. Symp. Soc. Exp. Biol.30, 233–255 (1976)

    Google Scholar 

  • Evans, M.H.: Tetrodotoxin, saxitoxin, and related substances: Their applications in neurobiology. Int. Rev. Neurobiol.15, 83–166 (1972)

    Google Scholar 

  • Fogel, M., Hastings, J.W.: Bioluminescence: Mechanism and mode of control of scintillon activity. Proc. Natl. Acad. Sci. USA69, 690–693 (1972)

    Google Scholar 

  • Fogel, M., Schmitter, R.E., Hastings, J.W.: On the physical identity of scintillons: Bioluminescent particles inGonyaulax polyedra. J. Cell Sci.11, 305–317 (1972)

    Google Scholar 

  • Gross, F.: Zur Biologie und Entwicklungsgeschichte vonNoctiluca miliaris. Arch. Protistenk.83, 178–196 (1934)

    Google Scholar 

  • Hastings, J.W.: Bioluminescence. Annu. Rev. Biochem.37, 597–630 (1968)

    Google Scholar 

  • Hastings, J.W., Vergin, M., DeSa, R.: Scintillons: The biochemistry of dinoflagellate bioluminescence. In: Bioluminescence in progress. Johnson, F.A., Haneda, Y. (eds.), pp. 301–329. Princeton, New Jersey: Princeton University Press 1966

    Google Scholar 

  • Kofoid, C.A., Swezy, O.: The free-living unarmored Dinoflagellata. Mem. Univ. Calif.5, 1–562 (1921)

    Google Scholar 

  • Narahashi, T.: Chemicals as tools in the study of excitable membranes. Physiol. Rev.54, 813–889 (1974)

    Google Scholar 

  • Nawata, T., Sibaoka, T.: Ionic composition and pH of the vacuolar sap in marine dinoflagellateNoctiluca. Plant Cell Physiol.17, 265–272 (1976)

    Google Scholar 

  • Nicol, J.A.C.: Observations on luminescence inNoctiluca. J. Mar. Biol. Ass. U.K.37, 535–549 (1958)

    Google Scholar 

  • Pratje, A.:Noctiluca miliaris Suriray. Beiträge zur Morphologie, Physiologie und Cytologie. I. Morphologie und Physiologie. Arch. Protistenk.42, 1–98 (1921)

    Google Scholar 

  • Sibaoka, T., Eckert, R.: An electrophysiological study of the tentacle-regulating potentials inNoctiluca. J. Exp. Biol.47, 447–459 (1967)

    Google Scholar 

  • Spencer, C.P.: The chemistry of ethylenediamine tetraacetic acid in sea water. J. Mar. Biol. Ass. U.K.37, 127–144 (1958)

    Google Scholar 

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This paper was based on a thesis by T. N. submitted to the graduate school of the Tohoku University in partial fullfilment of the requirements for the Ph. D. degree. This work was supported in part by a grant from the Ministry of Education to T. S. We are indebted to Prof. R. Eckert, University of California at Los Angeles, for helpful reading of the manuscript.

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Nawata, T., Sibaoka, T. Coupling between action potential and bioluminescence inNoctiluca: Effects of inorganic ions and pH in vacuolar sap. J. Comp. Physiol. 134, 137–149 (1979). https://doi.org/10.1007/BF00610472

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