全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...

Understanding Bioluminescence in Dinoflagellates—How Far Have We Come?

DOI: 10.3390/microorganisms1010003

Keywords: diel rhythms, functional diversity, luciferase, luciferin binding protein, gene, evolution, ecology, scintillon, predation defense

Full-Text   Cite this paper   Add to My Lib

Abstract:

Some dinoflagellates possess the remarkable genetic, biochemical, and cellular machinery to produce bioluminescence. Bioluminescent species appear to be ubiquitous in surface waters globally and include numerous cosmopolitan and harmful taxa. Nevertheless, bioluminescence remains an enigmatic topic in biology, particularly with regard to the organisms’ lifestyle. In this paper, we review the literature on the cellular mechanisms, molecular evolution, diversity, and ecology of bioluminescence in dinoflagellates, highlighting significant discoveries of the last quarter of a century. We identify significant gaps in our knowledge and conflicting information and propose some important research questions that need to be addressed to advance this research field.

References

[1]  Haddock, S.H.D.; Moline, M.A.; Case, J.F. Bioluminescence in the sea. Ann. Rev. Mar. Sci. 2010, 2, 443–493, doi:10.1146/annurev-marine-120308-081028.
[2]  Widder, E.A. Bioluminescence in the ocean: Origins of biological, chemical, and ecological diversity. Science 2010, 328, 704–708, doi:10.1126/science.1174269.
[3]  Wilson, T.; Hastings, J.W. Bioluminescence. Annu. Rev. Cell Dev. Biol. 1998, 14, 197–230, doi:10.1146/annurev.cellbio.14.1.197.
[4]  Hastings, J.W. Chemistry and control of luminescence in marine organisms. Bull. Mar. Sci. 1983, 33, 818–828.
[5]  Widder, E.A. Marine bioluminescence. Biosci. Explain. 2001, 1, 1–9.
[6]  Poupin, J.; Cussatlegras, A.S.; Geistdoerfer, P. Plancton Marin Bioluminescen; Rapport Scientifique du LOEN: Brest, France, 1999; p. 83.
[7]  Valiadi, M.; Iglesias-Rodriguez, M.D.; Amorim, A. Distribution and genetic diversity of the luciferase gene within marine dinoflagellates. J. Phycol. 2012, 48, 826–836, doi:10.1111/j.1529-8817.2012.01144.x.
[8]  Tett, P.B. The relation between dinoflagellates and the bioluminescence of sea water. J. Mar. Biol. Assoc. UK 1971, 51, 183–206, doi:10.1017/S002531540000655X.
[9]  Harvey, E.N. A History of Luminescence from the Earliest Times Until 1900: From the Earliest Times Until 1900; Dover Publications: Mineola, NY, USA, 1957; p. 692.
[10]  Lynch, R.V. The Occurence and Distribution of Surface Bioluminescence in the Oceans during 1966 through 1977; Naval Research Laboratory: Washington, DC, USA, 1978; p. 49.
[11]  Gomez, F. A quantitative review of the lifestyle, habitat and trophic diversity of dinoflagellates (Dinoflagellata, Alveolata). Syst. Biodivers. 2012, 10, 267–275, doi:10.1080/14772000.2012.721021.
[12]  DeSa, R.; Hastings, J.W. The characterization of scintillons. Bioluminescent particles from the marine dinoflagellate, Gonyaulax polyedra. J. Gen. Physiol. 1968, 51, 105–122, doi:10.1085/jgp.51.1.105.
[13]  Akimoto, H.; Wu, C.; Kinumi, T.; Ohmiya, Y. Biological rhythmicity in expressed proteins of the marine dinoflagellate Lingulodinium polyedrum demonstrated by chronological proteomics. Biochem. Biophys. Res. Commun. 2004, 315, 306–312, doi:10.1016/j.bbrc.2004.01.054.
[14]  Johnson, C.H.; Inoue, S.; Flint, A.; Hastings, J.W. Compartmentalization of algal bioluminescence—autofluorescence of bioluminescent particles in the dinoflagellate Gonyaulax as studied with image-intensified video microscopy and flow cytometry. J. Cell Biol. 1985, 100, 1435–1446, doi:10.1083/jcb.100.5.1435.
[15]  Knaust, R.; Urbig, T.; Li, L.M.; Taylor, W.; Hastings, J.W. The circadian rhythm of bioluminescence in Pyrocystis is not due to differences in the amount of luciferase: A comparative study of three bioluminescent marine dinoflagellates. J. Phycol. 1998, 34, 167–172.
[16]  Schmitter, R.E.; Njus, D.; Sulzman, F.M.; Gooch, V.D.; Hastings, J.W. Dinoflagellate bioluminescence—Comparative study of in vitro components. J. Cell. Physiol. 1976, 87, 123–134, doi:10.1002/jcp.1040870115.
[17]  Nicolas, M.T.; Sweeney, B.M.; Hastings, J.W. The ultrastructural localization of luciferase in three bioluminescent dinoflagellates, two species of Pyrocystis, and Noctiluca, using anti-luciferase and immunogold labelling. J. Cell Sci. 1987, 87, 189–196.
[18]  Fritz, L.; Morse, D.; Hastings, J.W. The circadian bioluminescence rhythm of Gonyaulax is related to daily variations in the number of light-emitting organelles. J. Cell Sci. 1990, 95, 321–328.
[19]  Seo, K.S.; Fritz, L. Cell ultrastructural changes correlate with circadian rhythms in Pyrocystis lunula (Pyrrophyta). J. Phycol. 2000, 36, 351–358.
[20]  Maldonado, E.M.; Latz, M.I. Shear-stress dependence of dinoflagellate bioluminescence. Biol. Bull. 2007, 212, 242–249, doi:10.2307/25066606.
[21]  Latz, M.I.; Bovard, M.; VanDelinder, V.; Segre, E.; Rohr, J.; Groisman, A. Bioluminescent response of individual dinoflagellate cells to hydrodynamic stress measured with millisecond resolution in a microfluidic device. J. Exp. Biol. 2008, 211, 2865–2875, doi:10.1242/jeb.011890.
[22]  Chen, A.K.; Latz, M.I.; Sobolewski, P.; Frangos, J.A. Evidence for the role of G-proteins in flow stimulation of dinoflagellate bioluminescence. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2007, 292, R2020–R2027, doi:10.1152/ajpregu.00649.2006.
[23]  Hardie, R.C.; Raghu, P. Visual transduction in Drosophila. Nature 2001, 413, 186–193, doi:10.1038/35093002.
[24]  Von Dassow, P.; Latz, M.I. The role of Ca2+ in stimulated bioluminescence of the dinoflagellate Lingulodinium polyedrum. J. Exp. Biol. 2002, 205, 2971–2986.
[25]  Fogel, M.; Hastings, J.W. Bioluminescence—Mechanism and mode of control of scintillon activity. Proc. Natl. Acad. Sci. USA 1972, 69, 690–693, doi:10.1073/pnas.69.3.690.
[26]  Smith, S.M.E.; Morgan, D.; Musset, B.; Cherny, V.V.; Place, A.R.; Hastings, J.W.; DeCoursey, T.E. Voltage-gated proton channel in a dinoflagellate. Proc. Natl. Acad. Sci. USA 2011, 108, 18162–18167.
[27]  Schultz, L.W.; Liu, L.; Cegielski, M.; Hastings, J.W. Crystal structure of a pH-regulated luciferase catalyzing the bioluminescent oxidation of an open tetrapyrrole. Proc. Natl. Acad. Sci. USA 2005, 102, 1378–1383, doi:10.1073/pnas.0409335102.
[28]  Shimomura, O. Bioluminescence: Chemical Principles and Methods; World Scientific: Singapore, Singapore, 2006; p. 470.
[29]  Wilson, T.; Hastings, J. Bioluminescence: Living Lights, Lights for Living; Harvard University Press: Cambridge, MA, USA, 2013; p. 185.
[30]  Liu, L.Y.; Wilson, T.; Hastings, J.W. Molecular evolution of dinoflagellate luciferases, enzymes with three catalytic domains in a single polypeptide. Proc. Natl. Acad. Sci. USA 2004, 101, 16555–16560, doi:10.1073/pnas.0407597101.
[31]  Li, L.; Hastings, J.W. The structure and organization of the luciferase gene in the photosynthetic dinoflagellate Gonyaulax polyedra. Plant Mol. Biol. 1998, 36, 275–284, doi:10.1023/A:1005941421474.
[32]  Liu, L.Y.; Hastings, J.W. Two different domains of the luciferase gene in the heterotrophic dinoflagellate Noctiluca scintillans occur as two separate genes in photosynthetic species. Proc. Natl. Acad. Sci. USA 2007, 104, 696–701, doi:10.1073/pnas.0607816103.
[33]  Li, L.; Hong, R.; Hastings, J.W. Three functional luciferase domains in a single polypeptide chain. Proc. Natl. Acad. Sci. USA 1997, 94, 8954–8958, doi:10.1073/pnas.94.17.8954.
[34]  Bae, Y.; Hastings, J. Cloning, sequencing and expression of dinoflagellate luciferase DNA from a marine alga. Gonyaulax polyedra. Biochim. Biophys. Acta Gene Struct. Expr. 1994, 1219, 449–456, doi:10.1016/0167-4781(94)90071-X.
[35]  Suzuki-Ogoh, C.; Wu, C.; Ohmiya, Y. C-terminal region of the active domain enhances enzymatic activity in dinoflagellate luciferase. Photochem. Photobiol. Sci. 2008, 7, 208–211, doi:10.1039/b713157g.
[36]  Li, L.; Liu, L.; Hong, R.; Robertson, D.; Hastings, J.W. N-terminal intramolecularly conserved histidines of three domains in Gonylaulax luciferase are responsible for loss of activity in the alkaline region. Biochemistry 2001, 40, 1844–1849.
[37]  Okamoto, O.K.; Liu, L.; Robertson, D.L.; Hastings, J.W. Members of a dinoflagellate luciferase gene family differ in synonymous substitution rates. Biochemistry 2001, 40, 15862–15868, doi:10.1021/bi011651q.
[38]  Liu, L.Y.; Hastings, J.W. Novel and rapidly diverging intergenic sequences between tandem repeats of the luciferase genes in seven dinoflagellate species. J. Phycol. 2006, 42, 96–103, doi:10.1111/j.1529-8817.2006.00165.x.
[39]  Swift, E.; Sullivan, J.M.; Batchelder, H.P.; van Keuren, J.; Vaillancourt, R.D.; Bidigare, R.R. Bioluminescent organisms and bioluminescence measurements in the North Atlantic Ocean near latitude 59.5 N, longitude 21 W. J. Geophys. Res. Oceans 1995, 100, 6527–6547, doi:10.1029/94JC01870.
[40]  Fogel, M.; Hastings, J.W. A substrate-binding protein in the Gonyaulax bioluminescence reaction. Arch. Biochem. Biophys. 1971, 142, 310–321, doi:10.1016/0003-9861(71)90289-X.
[41]  Erdner, D.L.; Anderson, D.M. Global transcriptional profiling of the toxic dinoflagellate Alexandrium fundyense using Massively Parallel Signature Sequencing. BMC Genomics 2006, 7, doi:10.1186/1471-2164-7-88.
[42]  Uribe, P.; Fuentes, D.; Valdés, J.; Shmaryahu, A.; Zú?iga, A.; Holmes, D.; Valenzuela, P.D.T. Preparation and analysis of an expressed sequence tag library from the toxic dinoflagellate Alexandrium catenella. Mar. Biotechnol. 2008, 10, 692–700, doi:10.1007/s10126-008-9107-8.
[43]  Hackett, J.D.; Scheetz, T.E.; Yoon, H.S.; Soares, M.B.; Bonaldo, M.F.; Casavant, T.L.; Bhattacharya, D. Insights into a dinoflagellate genome through expressed sequence tag analysis. BMC Genomics 2005, 6, doi:10.1186/1471-2164-6-80.
[44]  Jaeckisch, N.; Yang, I.; Wohlrab, S.; Gl?ckner, G.; Kroymann, J.; Vogel, H.; Cembella, A.; John, U. Comparative genomic and transcriptomic characterization of the toxigenic marine dinoflagellate Alexandrium ostenfeldii. PLoS One 2011, 6, e28012.
[45]  Machabée, S.; Wall, L.; Morse, D. Expression and genomic organization of a dinoflagellate gene family. Plant Mol. Biol. 1994, 25, 23–31, doi:10.1007/BF00024195.
[46]  Lee, D.H.; Mittag, M.; Sczekan, S.; Morse, D.; Hastings, J.W. Molecular cloning and genomic organization of a gene for luciferin-binding protein from the dinoflagellate Gonyaulax polyedra. J. Biol. Chem. 1993, 268, 8842–8850.
[47]  Morse, D.; Pappenheimer, A.M.; Hastings, J.W. Role of a luciferin-binding protein in the circadian bioluminescent reaction of Gonyaulax polyedra. J. Biol. Chem. 1989, 264, 11822–11826.
[48]  Toulza, E.; Shin, M.-S.; Blanc, G.; Audic, S.; Laabir, M.; Collos, Y.; Claverie, J.-M.; Grzebyk, D. Gene expression in proliferating cells of the dinoflagellate Alexandrium catenella (Dinophyceae). Appl. Environ. Microbiol. 2010, 76, 4521–4529, doi:10.1128/AEM.02345-09.
[49]  Tanikawa, N.; Akimoto, H.; Ogoh, K.; Chun, W.; Ohmiya, Y. Expressed sequence tag analysis of the dinoflagellate Lingulodinium polyedrum during dark phase. Photochem. Photobiol. 2004, 80, 31–35, doi:10.1562/2004-03-12-RA-110.1.
[50]  Dunlap, J.C.; Hastings, J.W. The biological clock in Gonyaulax controls luciferase activity by regulating turnover. J. Biol. Chem. 1981, 256, 10509–10518.
[51]  Fukuda, Y.; Endoh, H. Phylogenetic analyses of the dinoflagellate Noctiluca scintillans based on beta-tubulin and Hsp90 genes. Eur. J. Protistol. 2008, 44, 27–33, doi:10.1016/j.ejop.2007.07.001.
[52]  Hoppenrath, M.; Leander, B.S. Dinoflagellate phylogeny as inferred from heat shock protein 90 and ribosomal gene sequences. PLoS One 2010, 5, e13220, doi:10.1371/journal.pone.0013220.
[53]  Gomez, F.; Moreira, D.; Lopez-Garcia, P. Molecular phylogeny of noctilucoid dinoflagellates (Noctilucales, Dinophyceae). Protist 2010, 161, 466–478, doi:10.1016/j.protis.2009.12.005.
[54]  Orr, R.J.S.; Murray, S.A.; Stüken, A.; Rhodes, L.; Jakobsen, K.S. When naked became armored: An eight-gene phylogeny reveals monophyletic origin of theca in dinoflagellates. PLoS One 2012, 7, e50004.
[55]  Nakamura, H.; Kishi, Y.; Shimomura, O.; Morse, D.; Hastings, J.W. Structure of dinoflagellate luciferin and its enzymic and nonenzymic air-oxidation products. J. Am. Chem. Soc. 1989, 111, 7607–7611, doi:10.1021/ja00201a050.
[56]  Wu, C.; Akimoto, H.; Ohmiya, Y. Tracer studies on dinoflagellate luciferin with [15N]-glycine and [15N]-l-glutamic acid in the dinoflagellate Pyrocystis lunula. Tetrahedron Lett. 2003, 44, 1263–1266, doi:10.1016/S0040-4039(02)02815-0.
[57]  Topalov, G.; Kishi, Y. Chlorophyll catabolism leading to the skeleton of dinoflagellate and krill luciferins: Hypothesis and model studies. Angew. Chem. 2001, 40, 3892–3894, doi:10.1002/1521-3773(20011015)40:20<3892::AID-ANIE3892>3.0.CO;2-H.
[58]  Hamman, J.P.; Seliger, H.H. The mechanical triggering of bioluminescence in marine dinoflagellates: Chemical basis. J. Cell. Physiol. 1972, 80, 397–408, doi:10.1002/jcp.1040800310.
[59]  Yamaguchi, A.; Horiguchi, T. Culture of the heterotrophic dinoflagellate Protoperidinium crassipes (Dinophyceae) with noncellular food items. J. Phycol. 2008, 44, 1090–1092, doi:10.1111/j.1529-8817.2008.00547.x.
[60]  Shimomura, O. The roles of the two highly unstable components F and P involved in the bioluminescence of euphausiid shrimps. J. Biolumin. Chemilumin. 1995, 10, 91–101, doi:10.1002/bio.1170100205.
[61]  Marcinko, C.L.J.; Allen, J.T.; Poulton, A.J.; Painter, S.C.; Martin, A.P. Diurnal variations of dinoflagellate bioluminescence within the open-ocean north-east Atlantic. J. Plankton Res. 2013, 35, 177–190, doi:10.1093/plankt/fbs081.
[62]  Marcinko, C.L.J.; Painter, S.C.; Martin, A.P.; Allen, J.T. A review of the measurement and modelling of dinoflagellate bioluminescence. Prog. Oceanogr. 2013, 109, 117–129, doi:10.1016/j.pocean.2012.10.008.
[63]  Guiry, M.D.; Guiry, G.M. AlgaeBase World-Wide Electronic Publication; National University of Ireland: Galway, Ireland, 2013. Available online: http://www.algaebase.org (accessed on 28 April 2013).
[64]  Hastings, J.W. The Gonyaulax clock at 50: Translational control of circadian expression. Cold Spring Harbor Symp. Quant. Biol. 2007, 72, 141–144, doi:10.1101/sqb.2007.72.026.
[65]  Morse, D.; Milos, P.M.; Roux, E.; Hastings, J.W. Circadian regulation of bioluminescence in Gonyaulax involves translational control. Proc. Natl. Acad. Sci. USA 1989, 86, 172–176, doi:10.1073/pnas.86.1.172.
[66]  Mittag, M.; Li, L.; Hastings, J.W. The mRNA level of the circadian regulated Gonyaulax luciferase remains constant over the cycle. Chronobiol. Int. 1998, 1998, 93–98, doi:10.3109/07420529808998673.
[67]  Mittag, M.; Lee, D.H.; Hastings, J.W. Circadian expression of the luciferin-binding protein correlates with the binding of a protein to the 3′ untranslated region of its mRNA. Proc. Natl. Acad. Sci. USA 1994, 91, 5257–5261, doi:10.1073/pnas.91.12.5257.
[68]  Lapointe, M.; Morse, D. Reassessing the role of a 3′-UTR-binding translational inhibitor in regulation of circadian bioluminescence rhythm in the dinoflagellate Gonyaulax. Biol. Chem. 2008, 389, 13–19.
[69]  Johnson, C.H.; Roeber, J.F.; Hastings, J.W. Circadian changes in enzyme concentration account for rhythm of enzyme activity in Gonyaulax. Science 1984, 223, 1428–1430.
[70]  Esaias, W.E.; Curl, H.C.; Seliger, H.H. Action spectrum for a low intensity, rapid photoinhibition of mechanically stimulable bioluminescence in the marine dinoflagellates Gonyaulax catenella, G. acatenella, and G. tamarensis. J. Cell. Physiol. 1973, 82, 363–372, doi:10.1002/jcp.1040820306.
[71]  Hamman, J.P.; Biggley, W.H.; Seliger, H.H. Action spectrum for the photoinhibition of bioluminescence in the marine dinoflagellate Dissodinium lunula. Photochem. Photobiol. 1981, 33, 741–747, doi:10.1111/j.1751-1097.1981.tb05483.x.
[72]  Hamman, J.P.; Seliger, H.H. The chemical mimicking of the mechanical stimulation, photoinhibition, and recovery from photoinhibition of bioluminescence in the marine dinoflagellate, Gonyaulax polyedra. J. Cell. Physiol. 1982, 111, 315–319, doi:10.1002/jcp.1041110314.
[73]  Li, Y.Q.; Swift, E.; Buskey, E.J. Photoinhibition of mechanically stimulable bioluminescence in the heterotrophic dinoflagellate Protoperidinium depressum (Pyrrophyta). J. Phycol. 1996, 32, 974–982.
[74]  Sullivan, J.M.; Swift, E. Photoinhibition of mechanically stimulable bioluminescence in the autotrophic dinoflagellate Ceratium fusus (Pyrrophyta). J. Phycol. 1994, 30, 627–633.
[75]  Sweeney, B.M.; Haxo, F.T.; Hastings, J.W. Action spectra for two effects of light on luminescence in Gonyaulax polyedra. J. Gen. Physiol. 1959, 43, 285–299, doi:10.1085/jgp.43.2.285.
[76]  Buskey, E.J.; Strom, S.; Coulter, C. Biolumiscence of heterotrophic dinoflagellates from Texas coastal waters. J. Exp. Mar. Biol. Ecol. 1992, 159, 37–49, doi:10.1016/0022-0981(92)90256-A.
[77]  Raymond, J.A.; DeVries, A.L. Bioluminescence in McMurdo Sound, Antarctica. Limnol. Oceanogr. 1976, 21, 599–602, doi:10.4319/lo.1976.21.4.0599.
[78]  Hamman, J.P.; Biggley, W.H.; Seliger, H.H. Photoinhibition of stimulable bioluminescence in marine dinoflagellates. Photochem. Photobiol. 1981, 33, 909–914, doi:10.1111/j.1751-1097.1981.tb05511.x.
[79]  Lapota, D.; Young, D.K.; Bernstein, S.A.; Geiger, M.L.; Huddell, H.D.; Case, J.F. Diel bioluminescence in heterotrophic and photosynthetic marine dinoflagellates in an Arctic fjord. J. Mar. Biol. Assoc. UK 1992, 72, 733–744, doi:10.1017/S002531540006001X.
[80]  Batchelder, H.P.; Swift, E.; Keuren, J.R. Diel patterns of planktonic bioluminescence in the northern Sargasso Sea. Mar. Biol. 1992, 113, 329–339.
[81]  Biggley, W.H.; Swift, E.; Buchanan, R.J.; Seliger, H.H. Stimulable and spontaneous bioluminescence in the marine dinoflagellates Pyrodinium bahamense, Gonyaulax polyedra and Pyrocystis lunula. J. Gen. Physiol. 1969, 54, 96–122, doi:10.1085/jgp.54.1.96.
[82]  Krasnow, R.; Dunlap, J.; Taylor, W.; Hastings, J.W.; Vetterling, W.; Gooch, V. Circadian spontaneous bioluminescent glow and flashing of Gonyaulax polyedra. J. Comp. Physiol. B 1980, 138, 19–26, doi:10.1007/BF00688730.
[83]  Colepicolo, P.; Roenneberg, T.; Morse, D.; Taylor, W.R.; Hastings, J.W. Circadian regulation of bioluminescence in the dinoflagellate Pyrocystis lunula. J. Phycol. 1993, 29, 173–179.
[84]  Latz, M.I.; Lee, A.O. Spontaneous and stimulated bioluminescence of the dinoflagellate Ceratocorys horrida (Peridiniales). J. Phycol. 1995, 31, 120–132.
[85]  Eckert, R. Excitation and luminescence in Noctiluca miliaris. In Bio-luminescence in Progress; Johnson, F.H., Haneda, Y., Eds.; Princeton University Press: Princeton, NJ, USA; pp. 269–300.
[86]  Widder, E.; Case, J. Two flash forms in the bioluminescent dinoflagellate Pyrocystis fusiformis. J. Comp. Physiol. A 1981, 143, 43–52, doi:10.1007/BF00606067.
[87]  Schmidt, R.J.; Gooch, V.D.; Loeblich, A.R.; Hastings, J.W. Comparative study of luminescent and non-luminescent strains of Gonyaulax excavata (Pyrrhophyta). J. Phycol. 1978, 14, 5–9, doi:10.1111/j.1529-8817.1978.tb00624.x.
[88]  Cussatlegras, A.S.; Le Gal, P. Variability in the bioluminesence response of the dinoflagellate Pyrocystis lunula. J. Exp. Mar. Biol. Ecol. 2007, 343, 74–81, doi:10.1016/j.jembe.2006.11.009.
[89]  Buskey, E.J.; Swift, E. An encounter model to predict natural planktonic bioluminescence. Limnol. Oceanogr. 1990, 35, 1469–1485, doi:10.4319/lo.1990.35.7.1469.
[90]  Sweeney, B.M. Ultrastructure of Noctiluca miliaris (Pyrrophyta) with green flagellate symbionts. J. Phycol. 1978, 14, 116–120, doi:10.1111/j.1529-8817.1978.tb00643.x.
[91]  Eckert, R.; Reynolds, G. The subcellular origin of bioluminescence in Noctiluca miliaris. J. Gen. Physiol. 1967, 50, 1429–1458, doi:10.1085/jgp.50.5.1429.
[92]  Latz, M.I.; Case, J.F.; Gran, R.L. Excitation of bioluminescence by laminar fluid shear associated with simple Couette flow. Limnol. Oceanogr. 1994, 39, 1424–1439, doi:10.4319/lo.1994.39.6.1424.
[93]  von Dassow, P.; Bearon, R.N.; Latz, M.I. Bioluminescent response of the dinoflagellate Lingulodinium polyedrum to developing flow: Tuning of sensitivity and the role of desensitization in controlling a defensive behaviour of a planktonic cell. Limnol. Oceanogr. 2005, 50, 607–619, doi:10.4319/lo.2005.50.2.0607.
[94]  Sweeney, B.M. The loss of the circadian rhythm in photosynthesis in an old strain of Gonyaulax polyedra. Plant Physiol. 1986, 80, 978–981, doi:10.1104/pp.80.4.978.
[95]  Dickson, I. Bioluminescent Organelle Changes in Four Species of Dinoflagellates Using Confocal Laser Scanning Microscopy. MRes Dissertation, University of Southampton, Southampton, UK, 2008.
[96]  Swift, E.; Biggley, W.H.; Seliger, H.H. Species of oceanic dinoflagellates in genera Dissodinium and Pyrocystis—Interclonal and interspecific comparisons of color and photon yield of bioluminescence. J. Phycol. 1973, 9, 420–426.
[97]  Buskey, E.J.; Coulter, C.J.; Brown, S.L. Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi. Mar. Biol. 1994, 121, 373–380, doi:10.1007/BF00346747.
[98]  Sweeney, B.M. Variations of the Bioluminescence per Cell in Dinoflagellates. In Bioluminescence Current Perspectives; Nealson, K.H., Ed.; Burgess Publishing: Minneapolis, MN, USA, 1981; pp. 90–94.
[99]  Latz, M.I.; Jeong, H.J. Effect of red tide dinoflagellate diet and cannibalism on the bioluminescence of the heterotrophic dinoflagellates Protoperidinium spp. Mar. Ecol. Prog. Ser. 1996, 132, 275–285, doi:10.3354/meps132275.
[100]  Sullivan, J.M.; Swift, E. Photoenhancement of bioluminescence capacity in natural and laboratory populations of the autotrophic dinoflagellate Ceratium fusus (Ehrenb.) Dujardin. J. Geophys. Res. Oceans 1995, 100, 6565–6574, doi:10.1029/94JC01511.
[101]  Esaias, W.E.; Curl, H.C. Effect of dinoflagellate bioluminescence on copepod ingestion rates. Limnol. Oceanogr. 1972, 17, 901–905, doi:10.4319/lo.1972.17.6.0901.
[102]  White, H.H. Effects of dinoflagellate bioluminescence on the ingestion rates of herbivorous zooplankton. J. Exp. Mar. Biol. Ecol. 1979, 36, 217–224, doi:10.1016/0022-0981(79)90117-5.
[103]  Buskey, E.; Mills, L.; Swift, E. The effects of dinoflagellate bioluminescence on the swimming behavior of a marine copepod. Limnol. Oceanogr. 1983, 28, 575–579, doi:10.4319/lo.1983.28.3.0575.
[104]  Buskey, E.J.; Mann, C.G.; Swift, E. Photophobic responses of calanoid copepods: Possible adaptive value. J. Plankton Res. 1987, 9, 857–870, doi:10.1093/plankt/9.5.857.
[105]  Buskey, E.J.; Swift, E. Behavioral responses of oceanic zooplankton to simulated bioluminescence. Biol. Bull. 1985, 168, 263–275, doi:10.2307/1541239.
[106]  Burkenroad, M.D. A possible function of bioluminescence. J. Mar. Res. 1943, 5, 161–164.
[107]  Abrahams, M.V.; Townsend, L.D. Bioluminescence in dinoflgellates: A test of the burgular alarm hypothesis. Ecology 1993, 74, 258–260, doi:10.2307/1939521.
[108]  Mesinger, A.F.; Case, J.F. Dinoflagellate luminescence increases susceptibility of zooplankton to teleost predation. Mar. Biol. 1992, 112, 207–210, doi:10.1007/BF00702463.
[109]  Swift, E.; Lessard, E.J.; Biggley, W.H. Organisms associated with stimulated epipelagic bioluminescence in the Sargasso Sea and the Gulf Stream. J. Plankton Res. 1985, 7, 831–848, doi:10.1093/plankt/7.6.831.
[110]  Latz, M.I.; Frank, T.M.; Case, J.F. Spectral composition of bioluminescence of epipelagic organisms from the Sargasso Sea. Mar. Biol. 1988, 98, 441–446, doi:10.1007/BF00391120.
[111]  Neilson, D.J.; Latz, M.I.; Case, J.F. Temporal variability in the vertical structure of bioluminescence in the North Atlantic Ocean. J. Geophys. Res. Oceans 1995, 100, 6591–6603, doi:10.1029/94JC01448.
[112]  Baker, A.; Robbins, I.; Moline, M.A.; Iglesias-Rodriguez, M.D. Oligonucleotide primers for the detection of bioluminescent dinoflagellates reveal novel luciferase sequences and information on the molecular evolution of this gene. J. Phycol. 2008, 44, 419–428, doi:10.1111/j.1529-8817.2008.00474.x.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133