Scintillons

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Surf glowing blue in Southern California
Glowing dinoflagellate bloom

Marine dinoflagellates at night can emit blue light by bioluminescence, a process also called “the phosphorescence of the seas”. Light production in these single celled organisms is produced by small structures in the cytoplasm called scintillons. Among bioluminescent organisms, only dinoflagellates have scintillons.

In the dinoflagellates, the biochemical reaction that produces light involves a luciferase-catalysed oxidation of a linear tetrapyrrole called luciferin.[1]  The dinoflagellate Lingulodinium polyedra (previously called Gonyaulax polyedra) also contains a second protein called luciferin binding protein (LBP)[2] that has been proposed to protect luciferin from non-luminescent oxidation. Luciferin is released from LBP by a decrease in pH, and the same decreased pH also activates the luciferase.[3] Light production in the dinoflagellates occurs in bioluminescent organelles called scintillons and can be stimulated by agitation of the surrounding seawater.

The name scintillon was first used to describe cytoplasmic particles isolated from a bioluminescent species of dinoflagellate that were able to produce a flash of light in response to a decrease in pH.[4] Scintillons were first observed in L. polyedra by fluorescence microscopy,[5] where they appear as small blue dots close to the cell surface. This blue fluorescence is due to the presence of the bioluminescence reaction substrate, a naturally fluorescent molecule called luciferin.[6] When light production is stimulated by addition of dilute acid to the cells under the microscope, the site of light production corresponds to the location of the scintillons. Furthermore, the natural luciferin fluorescence is reduced after the light producing reaction.[5] 

Cells observed under the electron microscope after a technique involving rapid freezing of the cells followed by substitution of water with a polymer (Fast-freeze Fixation/Freeze Substitution) contain a large number of electron dense bodies around the cell periphery.[7] These structures correspond in size and location to the fluorescent bodies confirmed to be scintillons by their light emission, and they show colocalization of anti-luciferase and anti-LBP labeling meaning both bioluminescence proteins are found in the structures.[8] Scintillons appear as cytoplasmic drops hanging in the vacuolar space, as they are almost completely surrounded by the vacuolar membrane. This structure led to the proposal that a voltage gated proton channel in the vacuolar membrane could allow an action potential to be propagated along the vacuolar membrane.[7] This would in turn let protons enter into the cytoplasm around all the scintillons in the cells virtually simultaneously producing an intense but brief flash of light. Voltage gated proton channels were subsequently identified in a dinoflagellate confirming their predicted existence[9]

Scintillons have been extensively purified from L. polyedra by centrifugation, and these purified scintillon preparations contain luciferase and luciferin binding protein as the only detectable protein components.[10] The amount of luciferase,[11] LBP[12] and luciferin[13] all vary over the course of a daily (circadian) period, as do the number of scintillons in the cell.[14] These observations suggest that the circadian control of bioluminescence involves a daily synthesis and degradation of luciferase and LBP. When synthesized, these two proteins aggregate together and migrate to the vacuole membrane where LBP binds luciferin and the scintillons acquires an ability to produce light upon stimulation.

Scintillons are not identical in different species. Scintillons isolated from dinoflagellates belonging to the genus Pyrocystis such as P. lunula (previously Dissodinium lunula) or P. noctiluca are less dense than those of L. polyedra and do not contain LBP.[15] Little is known about the structure or composition of scintillons in species other than L. polyedra.

References[edit]

  1. ^ Nakamura, H.; Kishi, Y.; Shimomura, O.; Morse, D.; Hastings, J. W. (1990-01-09). "ChemInform Abstract: Structure of Dinoflagellate Luciferin and Its Enzymatic and Nonenzymatic Air-Oxidation Products". ChemInform. 21 (2): no. doi:10.1002/chin.199002330. ISSN 1522-2667.
  2. ^ Fogel, M.; Hastings, J. W. (January 1971). "A substrate-binding protein in the Gonyaulax bioluminescence reaction". Archives of Biochemistry and Biophysics. 142 (1): 310–321. doi:10.1016/0003-9861(71)90289-x. ISSN 0003-9861. PMID 5545485.
  3. ^ Morse, D.; Pappenheimer, A. M.; Hastings, J. W. (1989-07-15). "Role of a luciferin-binding protein in the circadian bioluminescent reaction of Gonyaulax polyedra". The Journal of Biological Chemistry. 264 (20): 11822–11826. ISSN 0021-9258. PMID 2745419.
  4. ^ DeSa, R.; Hastings, J. W. (January 1968). "The characterization of scintillons. Bioluminescent particles from the marine dinoflagellate, Gonyaulax polyedra". The Journal of General Physiology. 51 (1): 105–122. doi:10.1085/jgp.51.1.105. ISSN 0022-1295. PMC 2201157. PMID 5642469.
  5. ^ a b Johnson, C. H.; Inoué, S.; Flint, A.; Hastings, J. W. (May 1985). "Compartmentalization of algal bioluminescence: autofluorescence of bioluminescent particles in the dinoflagellate Gonyaulax as studied with image-intensified video microscopy and flow cytometry". The Journal of Cell Biology. 100 (5): 1435–1446. doi:10.1083/jcb.100.5.1435. ISSN 0021-9525. PMC 2113859. PMID 4039325.
  6. ^ Dunlap, J. C.; Hastings, J. W. (1981-02-17). "Biochemistry of dinoflagellate bioluminescence: purification and characterization of dinoflagellate luciferin from Pyrocystis lunula". Biochemistry. 20 (4): 983–989. doi:10.1021/bi00507a052. ISSN 0006-2960. PMID 7194111.
  7. ^ a b Nicolas, M. T.; Johnson, C. H.; Bassot, J. M.; Hastings, J. W. (September 1985). "Immunogold labeling of organelles in the bioluminescent dinoflagellate Gonyaulax polyedra with anti-luciferase antibody". Cell Biology International Reports. 9 (9): 797–802. doi:10.1016/0309-1651(85)90098-0. ISSN 0309-1651. PMID 3899376.
  8. ^ Nicolas, Marie-Thérèse; Morse, D.; Bassot, Jean-Marie; Hastings, J. Woodland (1991-06-01). "Colocalization of luciferin binding protein and luciferase to the scintillons ofGonyaulax polyedra revealed by double immunolabeling after fast-freeze fixation". Protoplasma. 160 (2–3): 159–166. doi:10.1007/bf01539967. ISSN 0033-183X.
  9. ^ Smith, Susan M. E.; Morgan, Deri; Musset, Boris; Cherny, Vladimir V.; Place, Allen R.; Hastings, J. Woodland; Decoursey, Thomas E. (2011-11-01). "Voltage-gated proton channel in a dinoflagellate". Proceedings of the National Academy of Sciences of the United States of America. 108 (44): 18162–18167. doi:10.1073/pnas.1115405108. ISSN 1091-6490. PMC 3207696. PMID 22006335.
  10. ^ Desjardins, M.; Morse, D. (March 1993). "The polypeptide components of scintillons, the bioluminescence organelles of the dinoflagellate Gonyaulax polyedra". Biochemistry and Cell Biology. 71 (3–4): 176–182. doi:10.1139/o93-028. ISSN 0829-8211. PMID 8398076.
  11. ^ Johnson, C. H.; Roeber, J. F.; Hastings, J. W. (1984-03-30). "Circadian changes in enzyme concentration account for rhythm of enzyme activity in gonyaulax". Science. 223 (4643): 1428–1430. doi:10.1126/science.223.4643.1428. ISSN 0036-8075. PMID 17746055.
  12. ^ Morse, D.; Milos, P. M.; Roux, E.; Hastings, J. W. (January 1989). "Circadian regulation of bioluminescence in Gonyaulax involves translational control". Proceedings of the National Academy of Sciences of the United States of America. 86 (1): 172–176. doi:10.1073/pnas.86.1.172. ISSN 0027-8424. PMC 286426. PMID 2911566.
  13. ^ Bode, V. C.; Desa, R.; Hastings, J. W. (1963-09-06). "Daily Rhythm of Luciferin Activity in Gonyaulax polyedra". Science. 141 (3584): 913–915. doi:10.1126/science.141.3584.913. ISSN 0036-8075. PMID 17844013.
  14. ^ Fritz, L.; Morse, D.; Hastings, J. W. (February 1990). "The circadian bioluminescence rhythm of Gonyaulax is related to daily variations in the number of light-emitting organelles". Journal of Cell Science. 95 ( Pt 2): 321–328. ISSN 0021-9533. PMID 2196272.
  15. ^ Schmitter, R. E.; Njus, D.; Sulzman, F. M.; Gooch, V. D.; Hastings, J. W. (January 1976). "Dinoflagellate bioluminescence: a comparative study of invitro components". Journal of Cellular Physiology. 87 (1): 123–134. doi:10.1002/jcp.1040870115. ISSN 0021-9541. PMID 1400.