Skip to main content
PMC home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1997 Nov;179(22):6979–6985. doi: 10.1128/jb.179.22.6979-6985.1997

Betaine and L-carnitine transport by Listeria monocytogenes Scott A in response to osmotic signals.

A Verheul 1, E Glaasker 1, B Poolman 1, T Abee 1
PMCID: PMC179637  PMID: 9371443

Abstract

The naturally occurring compatible solutes betaine and L-carnitine allow the food-borne pathogen Listeria monocytogenes to adjust to environments of high osmotic strength. Previously, it was demonstrated that L. monocytogenes possesses an ATP-dependent L-carnitine transporter (A. Verheul, F. M. Rombouts, R. R. Beumer, and T. Abee, J. Bacteriol. 177:3205-3212, 1995). The present study reveals that betaine and L-carnitine are taken up by separate highly specific transport systems and support a secondary transport mechanism for betaine uptake in L. monocytogenes. The initial uptake rates of betaine and L-carnitine are not influenced by an osmotic upshock, but the duration of transport of both osmolytes is directly related to the osmotic strength of the medium. Regulation of uptake of both betaine and L-carnitine is subject to inhibition by preaccumulated solute. Internal betaine inhibits not only transport of external betaine but also that of L-carnitine and, similarly, internal L-carnitine inhibits transport of both betaine and L-carnitine. The inhibition is alleviated upon osmotic upshock, which suggests that alterations in membrane structure are transmitted to the allosteric binding sites for betaine and L-carnitine of both transporters at the inner surface of the membrane. Upon osmotic downshock, betaine and L-carnitine are rapidly released by L. monocytogenes as a consequence of activation of a channel-like activity. The osmolyte-sensing mechanism described is new and is consistent with various unexplained observations of osmoregulation in other bacteria.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

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

  1. Amezaga M. R., Davidson I., McLaggan D., Verheul A., Abee T., Booth I. R. The role of peptide metabolism in the growth of Listeria monocytogenes ATCC 23074 at high osmolarity. Microbiology. 1995 Jan;141(Pt 1):41–49. doi: 10.1099/00221287-141-1-41. [DOI] [PubMed] [Google Scholar]
  2. BLIGH E. G., DYER W. J. A rapid method of total lipid extraction and purification. Can J Biochem Physiol. 1959 Aug;37(8):911–917. doi: 10.1139/o59-099. [DOI] [PubMed] [Google Scholar]
  3. Berrier C., Coulombe A., Szabo I., Zoratti M., Ghazi A. Gadolinium ion inhibits loss of metabolites induced by osmotic shock and large stretch-activated channels in bacteria. Eur J Biochem. 1992 Jun 1;206(2):559–565. doi: 10.1111/j.1432-1033.1992.tb16960.x. [DOI] [PubMed] [Google Scholar]
  4. Beumer R. R., Te Giffel M. C., Cox L. J., Rombouts F. M., Abee T. Effect of exogenous proline, betaine, and carnitine on growth of Listeria monocytogenes in a minimal medium. Appl Environ Microbiol. 1994 Apr;60(4):1359–1363. doi: 10.1128/aem.60.4.1359-1363.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Csonka L. N. Physiological and genetic responses of bacteria to osmotic stress. Microbiol Rev. 1989 Mar;53(1):121–147. doi: 10.1128/mr.53.1.121-147.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Farber J. M., Peterkin P. I. Listeria monocytogenes, a food-borne pathogen. Microbiol Rev. 1991 Sep;55(3):476–511. doi: 10.1128/mr.55.3.476-511.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Gerhardt P. N., Smith L. T., Smith G. M. Sodium-driven, osmotically activated glycine betaine transport in Listeria monocytogenes membrane vesicles. J Bacteriol. 1996 Nov;178(21):6105–6109. doi: 10.1128/jb.178.21.6105-6109.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Glaasker E., Konings W. N., Poolman B. Glycine betaine fluxes in Lactobacillus plantarum during osmostasis and hyper- and hypo-osmotic shock. J Biol Chem. 1996 Apr 26;271(17):10060–10065. doi: 10.1074/jbc.271.17.10060. [DOI] [PubMed] [Google Scholar]
  9. Glaasker E., Konings W. N., Poolman B. Osmotic regulation of intracellular solute pools in Lactobacillus plantarum. J Bacteriol. 1996 Feb;178(3):575–582. doi: 10.1128/jb.178.3.575-582.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Jung H., Jung K., Kleber H. P. L-carnitine metabolization and osmotic stress response in Escherichia coli. J Basic Microbiol. 1990;30(6):409–413. doi: 10.1002/jobm.3620300605. [DOI] [PubMed] [Google Scholar]
  11. Ko R., Smith L. T., Smith G. M. Glycine betaine confers enhanced osmotolerance and cryotolerance on Listeria monocytogenes. J Bacteriol. 1994 Jan;176(2):426–431. doi: 10.1128/jb.176.2.426-431.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Koo S. P., Higgins C. F., Booth I. R. Regulation of compatible solute accumulation in Salmonella typhimurium: evidence for a glycine betaine efflux system. J Gen Microbiol. 1991 Nov;137(11):2617–2625. doi: 10.1099/00221287-137-11-2617. [DOI] [PubMed] [Google Scholar]
  13. 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]
  14. Lamark T., Styrvold O. B., Strøm A. R. Efflux of choline and glycine betaine from osmoregulating cells of Escherichia coli. FEMS Microbiol Lett. 1992 Sep 15;75(2-3):149–154. doi: 10.1016/0378-1097(92)90395-5. [DOI] [PubMed] [Google Scholar]
  15. Landfald B., Strøm A. R. Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli. J Bacteriol. 1986 Mar;165(3):849–855. doi: 10.1128/jb.165.3.849-855.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Patchett R. A., Kelly A. F., Kroll R. G. Effect of sodium chloride on the intracellular solute pools of Listeria monocytogenes. Appl Environ Microbiol. 1992 Dec;58(12):3959–3963. doi: 10.1128/aem.58.12.3959-3963.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Patchett R. A., Kelly A. F., Kroll R. G. Transport of glycine-betaine by Listeria monocytogenes. Arch Microbiol. 1994;162(3):205–210. doi: 10.1007/BF00314476. [DOI] [PubMed] [Google Scholar]
  18. Pourkomailian B., Booth I. R. Glycine betaine transport by Staphylococcus aureus: evidence for feedback regulation of the activity of the two transport systems. Microbiology. 1994 Nov;140(Pt 11):3131–3138. doi: 10.1099/13500872-140-11-3131. [DOI] [PubMed] [Google Scholar]
  19. Premaratne R. J., Lin W. J., Johnson E. A. Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol. 1991 Oct;57(10):3046–3048. doi: 10.1128/aem.57.10.3046-3048.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Schleyer M., Schmid R., Bakker E. P. Transient, specific and extremely rapid release of osmolytes from growing cells of Escherichia coli K-12 exposed to hypoosmotic shock. Arch Microbiol. 1993;160(6):424–431. doi: 10.1007/BF00245302. [DOI] [PubMed] [Google Scholar]
  21. Smith L. T. Role of osmolytes in adaptation of osmotically stressed and chill-stressed Listeria monocytogenes grown in liquid media and on processed meat surfaces. Appl Environ Microbiol. 1996 Sep;62(9):3088–3093. doi: 10.1128/aem.62.9.3088-3093.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Stimeling K. W., Graham J. E., Kaenjak A., Wilkinson B. J. Evidence for feedback (trans) regulation of, and two systems for, glycine betaine transport by Staphylococcus aureus. Microbiology. 1994 Nov;140(Pt 11):3139–3144. doi: 10.1099/13500872-140-11-3139. [DOI] [PubMed] [Google Scholar]
  23. Verheul A., Rombouts F. M., Beumer R. R., Abee T. An ATP-dependent L-carnitine transporter in Listeria monocytogenes Scott A is involved in osmoprotection. J Bacteriol. 1995 Jun;177(11):3205–3212. doi: 10.1128/jb.177.11.3205-3212.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Whatmore A. M., Reed R. H. Determination of turgor pressure in Bacillus subtilis: a possible role for K+ in turgor regulation. J Gen Microbiol. 1990 Dec;136(12):2521–2526. doi: 10.1099/00221287-136-12-2521. [DOI] [PubMed] [Google Scholar]

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

RESOURCES