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. 1987 Dec;169(12):5801–5807. doi: 10.1128/jb.169.12.5801-5807.1987

Involvement of transport in Rhodobacter sphaeroides chemotaxis.

C J Ingham 1, J P Armitage 1
PMCID: PMC214150  PMID: 3500167

Abstract

The chemotactic response to a range of chemicals was investigated in the photosynthetic bacterium Rhodobacter sphaeroides, an organism known to lack conventional methyl-accepting sensory transduction proteins. Strong attractants included monocarboxylic acids and monovalent cations. Results suggest that the chemotactic response required the uptake of the chemoeffector, but not its metabolism. If a chemoeffector could block the uptake of another attractant, it also inhibited chemotaxis to that attractant. Sodium benzoate was not an attractant but was a competitive inhibitor of the propionate uptake system. Binding in an active uptake system was therefore insufficient to cause a chemotactic response. At different concentrations, benzoate either blocked propionate chemotaxis or reduced the sensitivity of propionate chemotaxis, an effect consistent with its role as a competitive inhibitor of uptake. Bacteria only showed chemotaxis to ammonium when grown under ammonia-limited conditions, which derepressed the ammonium transport system. Both chemotaxis and uptake were sensitive to the proton ionophore carbonyl cyanide m-chlorophenylhydrazone, suggesting an involvement of the proton motive force in chemotaxis, at least at the level of transport. There was no evidence for internal pH as a sensory signal. These results suggest a requirement for the uptake of attractants in chemotactic sensing in R. sphaeroides.

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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., Evans M. C. Membrane potential changes during chemotaxis of Rhodopseudomonas sphaeroides. FEBS Lett. 1979 Jun 1;102(1):143–146. doi: 10.1016/0014-5793(79)80946-1. [DOI] [PubMed] [Google Scholar]
  3. 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]
  4. 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]
  5. CLAYTON R. K. On the interplay of environmental factors affecting taxis and motility in Rhodospirillum rubrum. Arch Mikrobiol. 1958;29(2):189–212. doi: 10.1007/BF00409860. [DOI] [PubMed] [Google Scholar]
  6. Clancy M., Madill K. A., Wood J. M. Genetic and biochemical requirements for chemotaxis to L-proline in Escherichia coli. J Bacteriol. 1981 Jun;146(3):902–906. doi: 10.1128/jb.146.3.902-906.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Cordts M. L., Gibson J. Ammonium and methylammonium transport in Rhodobacter sphaeroides. J Bacteriol. 1987 Apr;169(4):1632–1638. doi: 10.1128/jb.169.4.1632-1638.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gibson J. Nutrient transport by anoxygenic and oxygenic photosynthetic bacteria. Annu Rev Microbiol. 1984;38:135–159. doi: 10.1146/annurev.mi.38.100184.001031. [DOI] [PubMed] [Google Scholar]
  9. Goulbourne E. A., Jr, Greenberg E. P. A voltage clamp inhibits chemotaxis of Spirochaeta aurantia. J Bacteriol. 1983 Feb;153(2):916–920. doi: 10.1128/jb.153.2.916-920.1983. [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. Harayama S., Iino T. Phototaxis and membrane potential in the photosynthetic bacterium Rhodospirillum rubrum. J Bacteriol. 1977 Jul;131(1):34–41. doi: 10.1128/jb.131.1.34-41.1977. [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. Hellingwerf K. J., Friedberg I., Lolkema J. S., Michels P. A., Konings W. N. Energy coupling of facilitated transport of inorganic ions in Rhodopseudomonas sphaeroides. J Bacteriol. 1982 Jun;150(3):1183–1191. doi: 10.1128/jb.150.3.1183-1191.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. 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]
  15. Jasper P. Potassium transport system of Rhodopseudomonas capsulata. J Bacteriol. 1978 Mar;133(3):1314–1322. doi: 10.1128/jb.133.3.1314-1322.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. 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]
  17. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  18. 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]
  19. 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]
  20. 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]
  21. Nicolay K., Lolkema J., Hellingwerf K. J., Kaptein R., Konings W. N. Quantitative agreement between the values for the light-induced delta pH in Rhodopseudomonas sphaeroides measured with automated follow-dialysis and 31P NMR. FEBS Lett. 1981 Jan 26;123(2):319–323. doi: 10.1016/0014-5793(81)80318-3. [DOI] [PubMed] [Google Scholar]
  22. Niwano M., Taylor B. L. Novel sensory adaptation mechanism in bacterial chemotaxis to oxygen and phosphotransferase substrates. Proc Natl Acad Sci U S A. 1982 Jan;79(1):11–15. doi: 10.1073/pnas.79.1.11. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Nowlin D. M., Nettleton D. O., Ordal G. W., Hazelbauer G. L. Chemotactic transducer proteins of Escherichia coli exhibit homology with methyl-accepting proteins from distantly related bacteria. J Bacteriol. 1985 Jul;163(1):262–266. doi: 10.1128/jb.163.1.262-266.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Repaske D. R., Adler J. Change in intracellular pH of Escherichia coli mediates the chemotactic response to certain attractants and repellents. J Bacteriol. 1981 Mar;145(3):1196–1208. doi: 10.1128/jb.145.3.1196-1208.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. SISTROM W. R. A requirement for sodium in the growth of Rhodopseudomonas spheroides. J Gen Microbiol. 1960 Jun;22:778–785. doi: 10.1099/00221287-22-3-778. [DOI] [PubMed] [Google Scholar]
  26. Segall J. E., Ishihara A., Berg H. C. Chemotactic signaling in filamentous cells of Escherichia coli. J Bacteriol. 1985 Jan;161(1):51–59. doi: 10.1128/jb.161.1.51-59.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shioi J., Taylor B. L. Oxygen taxis and proton motive force in Salmonella typhimurium. J Biol Chem. 1984 Sep 10;259(17):10983–10988. [PubMed] [Google Scholar]
  28. 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]
  29. Taylor B. L. Role of proton motive force in sensory transduction in bacteria. Annu Rev Microbiol. 1983;37:551–573. doi: 10.1146/annurev.mi.37.100183.003003. [DOI] [PubMed] [Google Scholar]
  30. Tso W. W., Adler J. Negative chemotaxis in Escherichia coli. J Bacteriol. 1974 May;118(2):560–576. doi: 10.1128/jb.118.2.560-576.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]

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