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Orientation by helical motion—III. Microorganisms can orient to stimuli by changing the direction of their rotational velocity

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Abstract

Organisms that move along helical trajectories change their net direction of motion largely by changing the direction, with respect to the body of the organism, of their rotational velocity (Crenshaw and Edelstein-Keshet, 1993,Bull. math. Biol. 55, 213–230). This paper demonstrates that an organism orients to a stimulus field, such as a chemical concentration gradient or a ray of light, if the components of its rotational velocity, with respect to the, body of the organism, are simple functions of the stimulus intensity encountered by the organism. For example, an organism can orient to a chemical concentration gradient if the rate at which it rotates around its anterior-posterior axis is proportional to the chemical concentration it encounters. Such an orientation can be either positive or negative. Furthermore, it is true taxis—orientation of the axis of helical motion is direct. It is neither a kinesis nor a phobic response—there is no random component to this mechanism of orientation.

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Literature

  • Berg, H. C. 1975. Chemotaxis in bacteria.A. Rev. Biophys. Bioengn 4 119–136.

    Article  Google Scholar 

  • Boscov, J. S. and M. E. Feinleib. 1979. Phototactic response ofChlamydomonas to flashes of light. II. Response of individual cells.Photochem. Photobiol. 30, 499–505.

    Google Scholar 

  • Brokaw, C. J. 1958a. Chemotaxis of bracken spermatozoids. Ph.D. thesis Cambridge, University, Cambridge, U.K.

    Google Scholar 

  • Brokaw, C. J. 1958b. Chemotaxis of bracken spermatozoids: Implication of electrochemical orientation.J. exp. Biol. 35, 197–212.

    Google Scholar 

  • Brokaw, C. J. 1959. Random and oriented movements of bracken spermatozoidsJ. cell. comp. Physiol. 54, 95–101.

    Article  Google Scholar 

  • Brokaw, C. J. 1974. Calcium and flagellar response during the chemotaxis of bracken spermatozids.J. cell. Physiol. 83, 151–158.

    Article  Google Scholar 

  • Brokaw, C. J. 1979. Calcium-induced asymmetrical beating of Triton-demembranated sea urchin sperm flagella.J. Cell Biol. 82, 401–411.

    Article  Google Scholar 

  • Brokaw, C. J., R. Josslin and L. Bobrow. 1974. Calcium ion regulation of flagellar beat symmetry in reactivated sea urchin spermatozoa.Biochem. Biophys. Res. Commun. 58, 795–800.

    Google Scholar 

  • Bullington, W. E. 1925. A study of spiral movement in the ciliate infusoria.Arch. Protistenk. 50, 219–275.

    Google Scholar 

  • Crenshaw, H. C. 1989. Kinematics of helical motion of microorganisms capable of motion with four degrees of freedom.Biophys. J. 56, 1029–1035. (Note correction inBiophys. J. 57, 1109.)

    Article  Google Scholar 

  • Crenshaw, H. C. 1990. Helical orientation: A novel mechanism for the orientation of microorganisms.Lect. Notes Biomath.89, 361–386.

    Google Scholar 

  • Crenshaw, H. C. 1993. Orientation by helical motion—I. Kinematics of the helical motion of organisms with up to six degrees of freedom.Bull. math. Biol. 55, 197–212.

    Article  MATH  Google Scholar 

  • Crenshaw, H. C. and L. Edelstein-Keshet. 1993. Orientation by helical motion—II. Changing the direction of the axis of motion.Bull. math. Biol. 55, 231–255.

    Article  MATH  Google Scholar 

  • Diehn, B. 1973. Phototaxis and sensory transduction inEuglena. Science 181, 1009–1015.

    Google Scholar 

  • Diehn, B., M. Feinleib, W. Haupt, E. Hildebrand, F. Lenci and W. Nultsch. 1977. Terminology of behavioral responses of motile microorganisms.Photochem. Photobiol. 26, 559–560.

    Google Scholar 

  • Fenchel, T. 1987.Ecology of Protozoa: The Biology of Free-living Phagotrophic Protists, p. 197. Madision, WI: Science Tech Publishers.

    Google Scholar 

  • Foster, K. W. and R. D. Smyth. 1980. Light antennas in phototactic algae.Microbiol. Rev. 44, 572–630.

    Google Scholar 

  • Foster, K. W., J. Saranak, N. Patel, G. Zarilli, M. Okabe, T. Kline and K. Nakanishi. 1984. A rhodopsin is the functional photoreceptor for phototaxis in the unicellular eukaryoteChlamydomonas.Nature 311, 756–759.

    Article  Google Scholar 

  • Fraenkel, G. S. and D. L. Gunn. 1940.The Orientation of Animals: Kineses, Taxes, and Compass Reactions 325 pp. Oxford, U.K.: Oxford University Press.

    Google Scholar 

  • Gibbons, B. H. and I. R. Gibbons. 1980. Calcium-induced quiescence in reactivated sea urchin sperm.J. Cell Biol. 84, 13–27.

    Article  Google Scholar 

  • Goldstein, S. F. 1977. Asymmetric waveforms in echinoderm sperm flagella.J. exp. Biol. 71, 157–170.

    Google Scholar 

  • Harz, H. and P. Hegemann. 1991. Rhodopsin-regulated calcium currents inChlamydomonas.Nature 351, 489–491.

    Article  Google Scholar 

  • van Houten, J. and R. R. Preston. 1988. Chemokinesis. InParamecium, H. D. Görtz (Ed.), pp. 282–300. New York, NY: Springer-Verlag.

    Google Scholar 

  • Jennings, H. S. 1904.Contributions to the Study of the Behavior of Lower Organisms. Carnegie Institute of Washington, Publication No. 16.

  • Kamiya, R. and G. B. Witman. 1984. Submicromolar levels of calcium control the balance of beating between the two flagella in demembranated models ofChlamydomonas.J. Cell Biol. 98, 97–107.

    Article  Google Scholar 

  • Kreimer, G. and M. Melkonian. 1990. Reflection confocal laser scanning microscopy of eyespots in flagellated green algae.Eur. J. Cell Biol. 53, 101–111.

    Google Scholar 

  • Ludwig, W. 1929. Untersuchungen über die schraubenbahnen niederer organismen.Z. vergl. Physiol. 9, 734–801.

    Article  Google Scholar 

  • Machemer, H. 1988a. Electrophysiology. InParamecium, H. D. Görtz (Ed.), pp. 185–215, New York, NY: Springer-Verlag.

    Google Scholar 

  • Machemer, H. 1988b. Motor control of cilia. InParamecium, H. D. Görtz (Ed.), pp. 216–235. New York, NY: Springer-Verlag.

    Google Scholar 

  • Machemer, H. 1989. Cellular behaviour modulated by ions: Electrophysiological implications.J. Protozool. 36, 463–487.

    Google Scholar 

  • Miller, R. L. 1985. Sperm chemo-orientation in the metazoa. InBiology of Fertilization, Vol. 2.Biology of the Sperm, C. B. Metz and A. Monroy (Ed), pp. 276–337. New York, NY: Academic Press.

    Google Scholar 

  • Miller, R. L. and C. J. Brokaw. 1970. Chemotactic turning behaviour ofTubularia spermatozoa.J. exp. Biol. 52, 699–706.

    Google Scholar 

  • Okuno, M. and C. J. Brokaw. 1981. Effects of Triton-extraction conditions on beat symmetry of sea urchin sperm flagella.Cell Motil. 1, 363–370.

    Article  Google Scholar 

  • Omoto, C. K. and C. J. Brokaw. 1985. Bending patterns of Chlamydomonas flagella. II. Calcium effects on reactivated Chlamydomonas flagella.Cell Motil. 5, 53–60.

    Article  Google Scholar 

  • Párducz, B. 1964. Swimming and its ciliary mechanism inOphryoglena sp.Acta Protozool. 2, 367–374.

    Google Scholar 

  • Rüffer, U. and W. Nultsch. 1987. Comparison of the beating of cis- and trans-flagella ofChlamydomonas cells held on micropipettes.Cell Motil. Cytoskel. 7, 87–93.

    Article  Google Scholar 

  • Rüffer, U. and W. Nultsch. 1990. Flagellar photoresponses ofChlamydomonas cells held on micropipettes: I. Change in flagellar beat frequency.Cell Motil. Cytoskel. 15, 162–167.

    Article  Google Scholar 

  • Rüffer, U. and W. Nultsch. 1991. Flagellar photoresponses ofChlamydomonas cells held on micropipettes: II. Change in flagellar beat pattern.Cell Motil. Cytoskel. 18, 269–278.

    Article  Google Scholar 

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Crenshaw, H.C. Orientation by helical motion—III. Microorganisms can orient to stimuli by changing the direction of their rotational velocity. Bltn Mathcal Biology 55, 231–255 (1993). https://doi.org/10.1007/BF02460304

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  • DOI: https://doi.org/10.1007/BF02460304

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