Skip to main content
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1993 Apr;175(7):2060–2066. doi: 10.1128/jb.175.7.2060-2066.1993

Amino acid transport in the thermophilic anaerobe Clostridium fervidus is driven by an electrochemical sodium gradient.

G Speelmans 1, B Poolman 1, W N Konings 1
PMCID: PMC204302  PMID: 8096211

Abstract

Amino acid transport was studied in membranes of the peptidolytic, thermophilic, anaerobic bacterium Clostridium fervidus. Uptake of the negatively charged amino acid L-glutamate, the neutral amino acid L-serine, and the positively charged amino acid L-arginine was examined in membrane vesicles fused with cytochrome c-containing liposomes. Artificial ion diffusion gradients were also applied to establish the specific driving forces for the individual amino acid transport systems. Each amino acid was driven by the delta psi and delta mu Na+/F and not by the Z delta pH. The Na+ stoichiometry was estimated from the amino acid-dependent 22Na+ efflux and Na(+)-dependent 3H-amino acid efflux. Serine and arginine were symported with 1 Na+ and glutamate with 2 Na+. C. fervidus membranes contain Na+/Na+ exchange activity, but Na+/H+ exchange activity could not be demonstrated.

Full text

PDF
2060

Selected References

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

  1. Booth I. R. Regulation of cytoplasmic pH in bacteria. Microbiol Rev. 1985 Dec;49(4):359–378. doi: 10.1128/mr.49.4.359-378.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Clement N. R., Gould J. M. Pyranine (8-hydroxy-1,3,6-pyrenetrisulfonate) as a probe of internal aqueous hydrogen ion concentration in phospholipid vesicles. Biochemistry. 1981 Mar 17;20(6):1534–1538. doi: 10.1021/bi00509a019. [DOI] [PubMed] [Google Scholar]
  3. Cunin R., Glansdorff N., Piérard A., Stalon V. Biosynthesis and metabolism of arginine in bacteria. Microbiol Rev. 1986 Sep;50(3):314–352. doi: 10.1128/mr.50.3.314-352.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. De Vrij W., Bulthuis R. A., Konings W. N. Comparative study of energy-transducing properties of cytoplasmic membranes from mesophilic and thermophilic Bacillus species. J Bacteriol. 1988 May;170(5):2359–2366. doi: 10.1128/jb.170.5.2359-2366.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. De Vrij W., Heyne R. I., Konings W. N. Characterization and application of a thermostable primary transport system: cytochrome-C oxidase from Bacillus stearothermophilus. Eur J Biochem. 1989 Jan 2;178(3):763–770. doi: 10.1111/j.1432-1033.1989.tb14507.x. [DOI] [PubMed] [Google Scholar]
  6. Deguchi Y., Yamato I., Anraku Y. Molecular cloning of gltS and gltP, which encode glutamate carriers of Escherichia coli B. J Bacteriol. 1989 Mar;171(3):1314–1319. doi: 10.1128/jb.171.3.1314-1319.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dibrov P. A. The role of sodium ion transport in Escherichia coli energetics. Biochim Biophys Acta. 1991 Feb 8;1056(3):209–224. doi: 10.1016/s0005-2728(05)80052-0. [DOI] [PubMed] [Google Scholar]
  8. Dimroth P. Mechanisms of sodium transport in bacteria. Philos Trans R Soc Lond B Biol Sci. 1990 Jan 30;326(1236):465–477. doi: 10.1098/rstb.1990.0025. [DOI] [PubMed] [Google Scholar]
  9. Dimroth P. Na(+)-coupled alternative to H(+)-coupled primary transport systems in bacteria. Bioessays. 1991 Sep;13(9):463–468. doi: 10.1002/bies.950130906. [DOI] [PubMed] [Google Scholar]
  10. Dimroth P. Sodium ion transport decarboxylases and other aspects of sodium ion cycling in bacteria. Microbiol Rev. 1987 Sep;51(3):320–340. doi: 10.1128/mr.51.3.320-340.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Driessen A. J., Poolman B., Kiewiet R., Konings W. Arginine transport in Streptococcus lactis is catalyzed by a cationic exchanger. Proc Natl Acad Sci U S A. 1987 Sep;84(17):6093–6097. doi: 10.1073/pnas.84.17.6093. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Escobales N., Figueroa J. Na+/Na+ exchange and Na+/H+ antiport in rabbit erythrocytes: two distinct transport systems. J Membr Biol. 1991 Feb;120(1):41–49. doi: 10.1007/BF01868589. [DOI] [PubMed] [Google Scholar]
  13. Hama H., Shimamoto T., Tsuda M., Tsuchiya T. Characterization of a novel L-serine transport system in Escherichia coli. J Bacteriol. 1988 May;170(5):2236–2239. doi: 10.1128/jb.170.5.2236-2239.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Hama H., Shimamoto T., Tsuda M., Tsuchiya T. Properties of a Na+-coupled serine-threonine transport system in Escherichia coli. Biochim Biophys Acta. 1987 Dec 11;905(2):231–239. doi: 10.1016/0005-2736(87)90451-2. [DOI] [PubMed] [Google Scholar]
  15. Heyne R. I., de Vrij W., Crielaard W., Konings W. N. Sodium ion-dependent amino acid transport in membrane vesicles of Bacillus stearothermophilus. J Bacteriol. 1991 Jan;173(2):791–800. doi: 10.1128/jb.173.2.791-800.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hinkle P. C., Kim J. J., Racker E. Ion transport and respiratory control in vesicles formed from cytochrome oxidase and phospholipids. J Biol Chem. 1972 Feb 25;247(4):1338–1339. [PubMed] [Google Scholar]
  17. Krulwich T. A., Hicks D. B., Seto-Young D., Guffanti A. A. The bioenergetics of alkalophilic bacilli. Crit Rev Microbiol. 1988;16(1):15–36. doi: 10.3109/10408418809104466. [DOI] [PubMed] [Google Scholar]
  18. 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]
  19. Nichols J. W., Deamer D. W. Net proton-hydroxyl permeability of large unilamellar liposomes measured by an acid-base titration technique. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2038–2042. doi: 10.1073/pnas.77.4.2038. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Russell J. B., Strobel H. J., Driessen A. J., Konings W. N. Sodium-dependent transport of neutral amino acids by whole cells and membrane vesicles of Streptococcus bovis, a ruminal bacterium. J Bacteriol. 1988 Aug;170(8):3531–3536. doi: 10.1128/jb.170.8.3531-3536.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Schellenberg G. D., Furlong C. E. Resolution of the multiplicity of the glutamate and aspartate transport systems of Escherichia coli. J Biol Chem. 1977 Dec 25;252(24):9055–9064. [PubMed] [Google Scholar]
  22. Skulachev V. P. The sodium cycle: a novel type of bacterial energetics. J Bioenerg Biomembr. 1989 Dec;21(6):635–647. doi: 10.1007/BF00762683. [DOI] [PubMed] [Google Scholar]
  23. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. Measurement of protein using bicinchoninic acid. Anal Biochem. 1985 Oct;150(1):76–85. doi: 10.1016/0003-2697(85)90442-7. [DOI] [PubMed] [Google Scholar]
  24. Speelmans G., de Vrij W., Konings W. N. Characterization of amino acid transport in membrane vesicles from the thermophilic fermentative bacterium Clostridium fervidus. J Bacteriol. 1989 Jul;171(7):3788–3795. doi: 10.1128/jb.171.7.3788-3795.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tolner B., Poolman B., Wallace B., Konings W. N. Revised nucleotide sequence of the gltP gene, which encodes the proton-glutamate-aspartate transport protein of Escherichia coli K-12. J Bacteriol. 1992 Apr;174(7):2391–2393. doi: 10.1128/jb.174.7.2391-2393.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Van Kessel J. S., Russell J. B. Energetics of arginine and lysine transport by whole cells and membrane vesicles of strain SR, a monensin-sensitive ruminal bacterium. Appl Environ Microbiol. 1992 Mar;58(3):969–975. doi: 10.1128/aem.58.3.969-975.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Verhoogt H. J., Smit H., Abee T., Gamper M., Driessen A. J., Haas D., Konings W. N. arcD, the first gene of the arc operon for anaerobic arginine catabolism in Pseudomonas aeruginosa, encodes an arginine-ornithine exchanger. J Bacteriol. 1992 Mar;174(5):1568–1573. doi: 10.1128/jb.174.5.1568-1573.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. de Vrij W., Bulthuis R. A., van Iwaarden P. R., Konings W. N. Mechanism of L-glutamate transport in membrane vesicles from Bacillus stearothermophilus. J Bacteriol. 1989 Feb;171(2):1118–1125. doi: 10.1128/jb.171.2.1118-1125.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES