Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1988 Dec;170(12):5673–5679. doi: 10.1128/jb.170.12.5673-5679.1988

Motility response of Rhodobacter sphaeroides to chemotactic stimulation.

P S Poole 1, J P Armitage 1
PMCID: PMC211668  PMID: 3263964

Abstract

Tethered rotating cells of Rhodobacter sphaeroides varied widely in their stopping frequency; 45% of cells showed no stops of longer than 1 s, whereas others showed stops of up to several seconds. Individual cells alternated between stops and rotation at a fairly constant rate, without continuous variation. Addition of the chemoattractant propionate to free-swimming cells of R. sphaeroides increased the mean population swimming speed from 15 to 23 microns s-1. After correction for nonmotile cells, the percentage swimming at less than 5 microns s-1 dropped from approximately 22 to 8, whereas the percentage swimming at greater than 50 microns s-1 increased from 6 to 15. However, cells already swimming did not swim faster after propionate addition; the increase in the mean population speed after propionate addition was caused by an increase in the mean run length between stops from 25 to 101 microns. The increased run length was the result of a drop in both the stopping frequency and the length of a stop. Addition of propionate over the range of 10 microM to 1 mM decreased the stopping frequency; this decrease was almost entirely blocked by benzoate, a competitive inhibitor of propionate transport. The chemoattractants acetate and potassium had the same effect as propionate on the distribution of stopping frequency, which demonstrated that this is a general behavioral response to chemotactic stimulation. Adaptation to propionate stimulation was slow and very variable, cultures frequently showing little adaptation over 30 min. This characteristic may be the result of the lack of a highly specific chemosensory system in R. sphaeroides.

Full text

PDF
5679

Images in this article

5674Image
on p.5674

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adler J., Epstein W. Phosphotransferase-system enzymes as chemoreceptors for certain sugars in Escherichia coli chemotaxis. Proc Natl Acad Sci U S A. 1974 Jul;71(7):2895–2899. doi: 10.1073/pnas.71.7.2895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Armitage J. P., Ingham C., Evans M. C. Role of proton motive force in phototactic and aerotactic responses of Rhodopseudomonas sphaeroides. J Bacteriol. 1985 Mar;161(3):967–972. doi: 10.1128/jb.161.3.967-972.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Armitage J. P., Macnab R. M. Unidirectional, intermittent rotation of the flagellum of Rhodobacter sphaeroides. J Bacteriol. 1987 Feb;169(2):514–518. doi: 10.1128/jb.169.2.514-518.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berg H. C., Brown D. A. Chemotaxis in Escherichia coli analysed by three-dimensional tracking. Nature. 1972 Oct 27;239(5374):500–504. doi: 10.1038/239500a0. [DOI] [PubMed] [Google Scholar]
  5. Boyd A., Simon M. Bacterial chemotaxis. Annu Rev Physiol. 1982;44:501–517. doi: 10.1146/annurev.ph.44.030182.002441. [DOI] [PubMed] [Google Scholar]
  6. Brouwer M., Elferink M. G., Robillard G. T. Phosphoenolpyruvate-dependent fructose phosphotransferase system of Rhodopseudomonas sphaeroides: purification and physicochemical and immunochemical characterization of a membrane-associated enzyme I. Biochemistry. 1982 Jan 5;21(1):82–88. doi: 10.1021/bi00530a015. [DOI] [PubMed] [Google Scholar]
  7. Clark A. J., Jackson J. B. The measurement of membrane potential during photosynthesis and during respiration in intact cells of Rhodopseudomonas capsulata by both electrochromism and by permeant ion redistribution. Biochem J. 1981 Nov 15;200(2):389–397. doi: 10.1042/bj2000389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Daniels G. A., Drews G., Saier M. H., Jr Properties of a Tn5 insertion mutant defective in the structural gene (fruA) of the fructose-specific phosphotransferase system of Rhodobacter capsulatus and cloning of the fru regulon. J Bacteriol. 1988 Apr;170(4):1698–1703. doi: 10.1128/jb.170.4.1698-1703.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Fosnaugh K., Greenberg E. P. Motility and chemotaxis of Spirochaeta aurantia: computer-assisted motion analysis. J Bacteriol. 1988 Apr;170(4):1768–1774. doi: 10.1128/jb.170.4.1768-1774.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Goulbourne E. A., Jr, Greenberg E. P. Chemotaxis of Spirochaeta aurantia: involvement of membrane potential in chemosensory signal transduction. J Bacteriol. 1981 Dec;148(3):837–844. doi: 10.1128/jb.148.3.837-844.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Götz R., Schmitt R. Rhizobium meliloti swims by unidirectional, intermittent rotation of right-handed flagellar helices. J Bacteriol. 1987 Jul;169(7):3146–3150. doi: 10.1128/jb.169.7.3146-3150.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Hazelbauer G. L., Harayama S. Sensory transduction in bacterial chemotaxis. Int Rev Cytol. 1983;81:33–70. doi: 10.1016/s0074-7696(08)62334-7. [DOI] [PubMed] [Google Scholar]
  13. Hess J. F., Oosawa K., Kaplan N., Simon M. I. Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell. 1988 Apr 8;53(1):79–87. doi: 10.1016/0092-8674(88)90489-8. [DOI] [PubMed] [Google Scholar]
  14. Hess J. F., Oosawa K., Matsumura P., Simon M. I. Protein phosphorylation is involved in bacterial chemotaxis. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7609–7613. doi: 10.1073/pnas.84.21.7609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Ingham C. J., Armitage J. P. Involvement of transport in Rhodobacter sphaeroides chemotaxis. J Bacteriol. 1987 Dec;169(12):5801–5807. doi: 10.1128/jb.169.12.5801-5807.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Jackson J. B., Crofts A. R. The high energy state in chromatophores from Rhodopseudomonas spheroides. FEBS Lett. 1969 Aug;4(3):185–189. doi: 10.1016/0014-5793(69)80230-9. [DOI] [PubMed] [Google Scholar]
  17. Kihara M., Macnab R. M. Cytoplasmic pH mediates pH taxis and weak-acid repellent taxis of bacteria. J Bacteriol. 1981 Mar;145(3):1209–1221. doi: 10.1128/jb.145.3.1209-1221.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Larsen S. H., Reader R. W., Kort E. N., Tso W. W., Adler J. Change in direction of flagellar rotation is the basis of the chemotactic response in Escherichia coli. Nature. 1974 May 3;249(452):74–77. doi: 10.1038/249074a0. [DOI] [PubMed] [Google Scholar]
  19. Laszlo D. J., Taylor B. L. Aerotaxis in Salmonella typhimurium: role of electron transport. J Bacteriol. 1981 Feb;145(2):990–1001. doi: 10.1128/jb.145.2.990-1001.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Macnab R. M., Aizawa S. Bacterial motility and the bacterial flagellar motor. Annu Rev Biophys Bioeng. 1984;13:51–83. doi: 10.1146/annurev.bb.13.060184.000411. [DOI] [PubMed] [Google Scholar]
  21. Manson M. D., Tedesco P., Berg H. C., Harold F. M., Van der Drift C. A protonmotive force drives bacterial flagella. Proc Natl Acad Sci U S A. 1977 Jul;74(7):3060–3064. doi: 10.1073/pnas.74.7.3060. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Nicolay K., Kaptein R., Hellingwerf K. J., Konings W. N. 31P nuclear magnetic resonance studies of energy transduction in Rhodopseudomonas sphaeroides. Eur J Biochem. 1981 May;116(1):191–197. doi: 10.1111/j.1432-1033.1981.tb05318.x. [DOI] [PubMed] [Google Scholar]
  23. Oosawa K., Hess J. F., Simon M. I. Mutants defective in bacterial chemotaxis show modified protein phosphorylation. Cell. 1988 Apr 8;53(1):89–96. doi: 10.1016/0092-8674(88)90490-4. [DOI] [PubMed] [Google Scholar]
  24. Parkinson J. S. Protein phosphorylation in bacterial chemotaxis. Cell. 1988 Apr 8;53(1):1–2. doi: 10.1016/0092-8674(88)90478-3. [DOI] [PubMed] [Google Scholar]
  25. Saier M. H., Jr, Feucht B. U., Roseman S. Phosphoenolpyruvate-dependent fructose phosphorylation in photosynthetic bacteria. J Biol Chem. 1971 Dec 25;246(24):7819–7821. [PubMed] [Google Scholar]
  26. Shioi J., Dang C. V., Taylor B. L. Oxygen as attractant and repellent in bacterial chemotaxis. J Bacteriol. 1987 Jul;169(7):3118–3123. doi: 10.1128/jb.169.7.3118-3123.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sockett R. E., Armitage J. P., Evans M. C. Methylation-independent and methylation-dependent chemotaxis in Rhodobacter sphaeroides and Rhodospirillum rubrum. J Bacteriol. 1987 Dec;169(12):5808–5814. doi: 10.1128/jb.169.12.5808-5814.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Stock J. B., Maderis A. M., Koshland D. E., Jr Bacterial chemotaxis in the absence of receptor carboxylmethylation. Cell. 1981 Nov;27(1 Pt 2):37–44. doi: 10.1016/0092-8674(81)90358-5. [DOI] [PubMed] [Google Scholar]
  29. Stock J., Kersulis G., Koshland D. E., Jr Neither methylating nor demethylating enzymes are required for bacterial chemotaxis. Cell. 1985 Sep;42(2):683–690. doi: 10.1016/0092-8674(85)90125-4. [DOI] [PubMed] [Google Scholar]
  30. Weis R. M., Koshland D. E., Jr Reversible receptor methylation is essential for normal chemotaxis of Escherichia coli in gradients of aspartic acid. Proc Natl Acad Sci U S A. 1988 Jan;85(1):83–87. doi: 10.1073/pnas.85.1.83. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Wylie D., Stock A., Wong C. Y., Stock J. Sensory transduction in bacterial chemotaxis involves phosphotransfer between Che proteins. Biochem Biophys Res Commun. 1988 Mar 15;151(2):891–896. doi: 10.1016/s0006-291x(88)80365-6. [DOI] [PubMed] [Google Scholar]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES