Reuse & Permissions

It is not necessary to obtain permission to reuse this article or its components as it is available under the terms of the Creative Commons Attribution 4.0 International license. This license permits unrestricted use, distribution, and reproduction in any medium, provided attribution to the author(s) and the published article's title, journal citation, and DOI are maintained. Please note that some figures may have been included with permission from other third parties. It is your responsibility to obtain the proper permission from the rights holder directly for these figures.

Export citation

Export citation

Choose format for download:

Download Citation
  • Featured in Physics
  • Editors' Suggestion
  • Open Access

Stress-Induced Dinoflagellate Bioluminescence at the Single Cell Level

Maziyar Jalaal1, Nico Schramma1,2, Antoine Dode1,3, Hélène de Maleprade1, Christophe Raufaste1,4, and Raymond E. Goldstein1,*

  • 1Department of Applied Mathematics and Theoretical Physics, University of Cambridge, Cambridge CB3 0WA, United Kingdom
  • 2Max Planck Institute for Dynamics and Self-Organization, 37077 Göttingen, Germany
  • 3LadHyX, UMR 7646 du CNRS, École polytechnique, 91120 Palaiseau, France
  • 4Université Côte d’Azur, CNRS, Institut de Physique de Nice, CNRS, 06100 Nice, France

  • *R.E.Goldstein@damtp.cam.ac.uk

Phys. Rev. Lett. 125, 028102 – Published 6 July, 2020

DOI: https://doi.org/10.1103/PhysRevLett.125.028102

Abstract

One of the characteristic features of many marine dinoflagellates is their bioluminescence, which lights up nighttime breaking waves or seawater sliced by a ship’s prow. While the internal biochemistry of light production by these microorganisms is well established, the manner by which fluid shear or mechanical forces trigger bioluminescence is still poorly understood. We report controlled measurements of the relation between mechanical stress and light production at the single cell level, using high-speed imaging of micropipette-held cells of the marine dinoflagellate Pyrocystis lunula subjected to localized fluid flows or direct indentation. We find a viscoelastic response in which light intensity depends on both the amplitude and rate of deformation, consistent with the action of stretch-activated ion channels. A phenomenological model captures the experimental observations.

View figure in article

Physics Subject Headings (PhySH)

Focus

A Light Squeeze

Published 6 July, 2020

Experiments detail how mechanical stress triggers marine microbes to light up.

See more in Physics

Article Text

Supplemental Material

References (35)

  1. E. N. Harvey, The Nature of Animal Light (J. B. Lippincott Company, Philadelphia, 1920).
  2. C. Darwin, in Journal of Researches into the Geology and Natural History of the Various Countries Visited by H.M.S. Beagle, Under the Command of Captain Fitzroy, R.N. from 1832 to 1836 (Henry Colburn, London, 1839), p. 191.
  3. S. H. D. Haddock, M. A. Moline, and J. F. Case, Bioluminescence in the sea, Annu. Rev. Mar. Sci. 2, 443 (2010).
  4. T. Wilson and W. J. Hastings, Bioluminescence, Annu. Rev. Cell Dev. Biol. 14, 197 (1998); M. Valiadi and D. Iglesias-Rodriguez, Understanding bioluminescence in dinoflagellates—How far have we come?, Microorganisms 1, 3 (2013).
  5. M. Fogel and J. W. Hastings, Bioluminescence: Mechanism and mode of control of scintillon activity, Proc. Natl. Acad. Sci. U.S.A. 69, 690 (1972).
  6. W. H. Biggley, E. Swift, R. J. Buchanan, and H. H. Seliger, Stimulable and spontaneous bioluminescence in the marine dinoflagellates, Pyrodinium bahamense, Gonyaulax polyedra, and Pyrocystis lunula, J. Gen. Physiol. 54, 96 (1969); G. B. Deane, M. D. Stokes, and M. I. Latz, Bubble stimulation efficiency of dinoflagellate bioluminescence, Luminescence 31, 270 (2016).
  7. M. I. Latz, J. F. Case, and R. L. Gran, Excitation of bioluminescence by laminar fluid shear associated with simple Couette flow, Limnol. Oceanogr. 39, 1424 (1994); E. M. Maldonado and M. I. Latz, Shear-stress dependence of dinoflagellate bioluminescence, Biol. Bull. 212, 242 (2007).
  8. A.-S. Cussatlegras and P. Le Gal, Variability in the bioluminescence response of the dinoflagellate Pyrocystis lunula, J. Exp. Mar. Biol. Ecol. 343, 74 (2007).
  9. M. I. Latz, J. Rohr, and J. Hoyt, A novel flow visualization technique using bioluminescent marine plankton. I. Laboratory studies, IEEE J. Oceanic Eng. 20, 147 (1995).
  10. M. I. Latz, A. R. Juhl, A. M. Ahmed, S. E. Elghobashi, and J. Rohr, Hydrodynamic stimulation of dinoflagellate bioluminescence: A computational and experimental study, J. Exp. Biol. 207, 1941 (2004).
  11. M. I. Latz, M. Bovard, V. VanDelinder, E. Segre, J. Rohr, and A. Groisman, Bioluminescent response of individual dinoflagellate cells to hydrodynamic stress measured with millisecond resolution in a microfluidic device, J. Exp. Biol. 211, 2865 (2008).
  12. B. Tesson and M. I. Latz, Mechanosensitivity of a rapid bioluminescence reporter system assessed by atomic force microscopy, Biophys. J. 108, 1341 (2015).
  13. J. Rohr, J. Allen, J. Losee, and M. I. Latz, The use of bioluminescence as a flow diagnostic, Phys. Lett. A 228, 408 (1997).
  14. E. Foti, C. Faraci, R. Foti, and G. Bonanno, On the use of bioluminescence for estimating shear stresses over a rippled seabed, Meccanica 45, 881 (2010).
  15. J. Hauslage, V. Cevik, and R. Hemmersbach, Pyrocystis noctiluca represents an excellent bioassay for shear forces induced in ground-based microgravity simulators (clinostat and random positioning machine), npj Microgravity 3, 12 (2017).
  16. G. B. Deane and M. D. Stokes, A quantitative model for flow-induced bioluminescence in dinoflagellates, J. Theor. Biol. 237, 147 (2005).
  17. K. Jin, J. C. Klima, G. Deane, M. D. Stokes, and M. I. Latz, Pharmacological investigation of the bioluminescence signaling pathway of the dinoflagellat Lingulodinium polyedrum: Evidence for the role of stretch-activated ion channels, J. Phycol. 49, 733 (2013).
  18. C. Kung, A possible unifying principle for mechanosensation, Nature (London) 436, 647 (2005).
  19. J. D. Hackett, D. M. Anderson, D. L. Erdner, and D. Bhattacharya, Dinoflagellates: A remarkable evolutionary experiment, Am. J. Bot. 91, 1523 (2004); C. Fajardo, F. Amil-Ruiz, C. Fuentes-Almagro, M. De Donato, G. Martinez-Rodriguez, A. Escobar-Niño, R. Carrasco, J. Miguel Mancera, and F. Javier Fernandez-Acero, An “omic” approach to Pyrocystis lunula: New insights related with this bioluminescent dinoflagellate, J. Proteomics 209, 103502 (2019).
  20. The Culture Collection of Algae and Protozoa (CCAP), https://www.ccap.ac.uk/index.htm.
  21. R. R. L. Guillard and P. E. Hargraves, Stichochrysis immobilis is a diatom, not a chrysophyte, Phycologia 32, 234 (1993).
  22. E. Swift and W. R. Taylor, Bioluminescence and chloroplast movement in the dinoflagellate Pyrocystis Lunula, J. Phycol. 3, 77 (1967).
  23. P. Colepicolo, T. Roenneberg, D. Morse, W. R. Taylor, and J. W. Hastings, Circadian regulation of bioluminescence in the dinoflagellate Pyrocystis Lunula, J. Phycol. 29, 173 (1993).
  24. See Supplemental Material at http://link.aps.org/supplemental/10.1103/PhysRevLett.125.028102 for further experimental details and videos.
  25. E. A. Widder and J. F. Case, Two flash forms in the bioluminescent dinoflagellate, Pyrocystis fusiformis, J. Comp. Physiol. 143, 43 (1981).
  26. E. Swift and C. C. Remsen, The cell wall of Pyrocystis spp. (Dinococcales), J. Phycol. 6, 79 (1970).
  27. R. A. Fensome, F. J. R. Taylor, G. Norris, W. A. S. Sarjeant, D. I. Wharton, and G. L. Williams, A Classification of Living and Fossil Dinoflagellates (Sheridan Press, Pennsylvania, 1993), Micropaleontology, Spec. Pub. No. 7.
  28. K. S. Seo and L. Fritz, Cell-wall morphology correlated with vertical migration in the non-motile marine dinoflagellate Pyrocystis noctiluca, Mar. Biol. 137, 589 (2000).
  29. E. Swift and E. G. Durbin, Similarities in the asexual reproduction of the oceanic dinoflagellates, Pyrocystis fusiformis, Pyrocystis lunula, and Pyrocystis noctiluca, J. Phycol. 7, 89 (1971).
  30. L. D. Landau and E. M. Lifshitz, in Theory of Elasticity, 3rd ed. (Elsevier, Amsterdam, 1986), p. 15.
  31. K. S. Seo and L. Fritz, Cell ultrastructural changes correlate with circadian rhythms in Pyrocystis lunula (Pyrrophyta), J. Phycol. 36, 351 (2000).
  32. A. Goldbeter, G. Dupont, and M. J. Berridge, Minimal model for signal-induced Ca2+ oscillations and for their frequency encoding through protein phosphorylation, Proc. Natl. Acad. Sci. U.S.A. 87, 1461 (1990).
  33. P. A. Spiro, J. S. Parkinson, and H. G. Othmer, A model of excitation and adaptation in bacterial chemotaxis, Proc. Natl. Acad. Sci. U.S.A. 94, 7263 (1997).
  34. K. Drescher, R. E. Goldstein, and I. Tuval, Fidelity of adaptive phototaxis, Proc. Natl. Acad. Sci. U.S.A. 107, 11171 (2010).
  35. R. Trans-Son-Tay, S. P. Sutera, G. I. Zahalak, and P. R. Rao, Membranes stresses and internal pressure in a red blood cell freely suspended in a shear flow, Biophys. J. 51, 915 (1987); A. Théry, M. Jalaal, E. Lauga, and R. E. Goldstein (to be published).

Outline

Information

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation