Skip to main content

Some NLM-NCBI services and products are experiencing heavy traffic, which may affect performance and availability. We apologize for the inconvenience and appreciate your patience. For assistance, please contact our Help Desk at info@ncbi.nlm.nih.gov.

Journal of Bacteriology logoLink to Journal of Bacteriology
. 1995 Aug;177(16):4652–4657. doi: 10.1128/jb.177.16.4652-4657.1995

Specificity of peptide transport systems in Lactococcus lactis: evidence for a third system which transports hydrophobic di- and tripeptides.

C Foucaud 1, E R Kunji 1, A Hagting 1, J Richard 1, W N Konings 1, M Desmazeaud 1, B Poolman 1
PMCID: PMC177229  PMID: 7642491

Abstract

A proton motive force-driven di-tripeptide carrier protein (DtpT) and an ATP-dependent oligopeptide transport system (Opp) have been described for Lactococcus lactis MG1363. Using genetically well-defined mutants in which dtpT and/or opp were inactivated, we have now established the presence of a third peptide transport system (DtpP) in L. lactis. The specificity of DtpP partially overlaps that of DtpT. DtpP transports preferentially di- and tripeptides that are composed of hydrophobic (branched-chain amino acid) residues, whereas DtpT has a higher specificity for more-hydrophilic and charged peptides. The toxic dipeptide L-phenylalanyl-beta-chloro-L-alanine has been used to select for a di-tripeptide transport-negative mutant with the delta dtpT strain as a genetic background. This mutant is unable to transport di- and tripeptides but still shows uptake of amino acids and oligopeptides. The DtpP system is induced in the presence of di- and tripeptides containing branched-chain amino acids. The use of ionophores and metabolic inhibitors suggests that, similar to Opp, DtpP-mediated peptide transport is driven by ATP or a related energy-rich phosphorylated intermediate.

Full Text

The Full Text of this article is available as a PDF (281.0 KB).

Selected References

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

  1. Andrews J. C., Blevins T. C., Short S. A. Regulation of peptide transport in Escherichia coli: induction of the trp-linked operon encoding the oligopeptide permease. J Bacteriol. 1986 Feb;165(2):428–433. doi: 10.1128/jb.165.2.428-433.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Driessen A. J., de Jong S., Konings W. N. Transport of branched-chain amino acids in membrane vesicles of Streptococcus cremoris. J Bacteriol. 1987 Nov;169(11):5193–5200. doi: 10.1128/jb.169.11.5193-5200.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Gasson M. J. Plasmid complements of Streptococcus lactis NCDO 712 and other lactic streptococci after protoplast-induced curing. J Bacteriol. 1983 Apr;154(1):1–9. doi: 10.1128/jb.154.1.1-9.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Goodell E. W., Higgins C. F. Uptake of cell wall peptides by Salmonella typhimurium and Escherichia coli. J Bacteriol. 1987 Aug;169(8):3861–3865. doi: 10.1128/jb.169.8.3861-3865.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Hagting A., Kunji E. R., Leenhouts K. J., Poolman B., Konings W. N. The di- and tripeptide transport protein of Lactococcus lactis. A new type of bacterial peptide transporter. J Biol Chem. 1994 Apr 15;269(15):11391–11399. [PubMed] [Google Scholar]
  6. Higgins C. F. ABC transporters: from microorganisms to man. Annu Rev Cell Biol. 1992;8:67–113. doi: 10.1146/annurev.cb.08.110192.000435. [DOI] [PubMed] [Google Scholar]
  7. Jamieson D. J., Higgins C. F. Anaerobic and leucine-dependent expression of a peptide transport gene in Salmonella typhimurium. J Bacteriol. 1984 Oct;160(1):131–136. doi: 10.1128/jb.160.1.131-136.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Juillard V., Laan H., Kunji E. R., Jeronimus-Stratingh C. M., Bruins A. P., Konings W. N. The extracellular PI-type proteinase of Lactococcus lactis hydrolyzes beta-casein into more than one hundred different oligopeptides. J Bacteriol. 1995 Jun;177(12):3472–3478. doi: 10.1128/jb.177.12.3472-3478.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kunji E. R., Hagting A., De Vries C. J., Juillard V., Haandrikman A. J., Poolman B., Konings W. N. Transport of beta-casein-derived peptides by the oligopeptide transport system is a crucial step in the proteolytic pathway of Lactococcus lactis. J Biol Chem. 1995 Jan 27;270(4):1569–1574. doi: 10.1074/jbc.270.4.1569. [DOI] [PubMed] [Google Scholar]
  10. Kunji E. R., Smid E. J., Plapp R., Poolman B., Konings W. N. Di-tripeptides and oligopeptides are taken up via distinct transport mechanisms in Lactococcus lactis. J Bacteriol. 1993 Apr;175(7):2052–2059. doi: 10.1128/jb.175.7.2052-2059.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. 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]
  12. Manning J. M., Merrifield N. E., Jones W. M., Gotschlich E. C. Inhibition of bacterial growth by beta-chloro-D-alanine. Proc Natl Acad Sci U S A. 1974 Feb;71(2):417–421. doi: 10.1073/pnas.71.2.417. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Molenaar D., Hagting A., Alkema H., Driessen A. J., Konings W. N. Characteristics and osmoregulatory roles of uptake systems for proline and glycine betaine in Lactococcus lactis. J Bacteriol. 1993 Sep;175(17):5438–5444. doi: 10.1128/jb.175.17.5438-5444.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Payne J. W., Smith M. W. Peptide transport by micro-organisms. Adv Microb Physiol. 1994;36:1–80. doi: 10.1016/s0065-2911(08)60176-9. [DOI] [PubMed] [Google Scholar]
  15. Poolman B., Driessen A. J., Konings W. N. Regulation of arginine-ornithine exchange and the arginine deiminase pathway in Streptococcus lactis. J Bacteriol. 1987 Dec;169(12):5597–5604. doi: 10.1128/jb.169.12.5597-5604.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Poolman B., Driessen A. J., Konings W. N. Regulation of solute transport in streptococci by external and internal pH values. Microbiol Rev. 1987 Dec;51(4):498–508. doi: 10.1128/mr.51.4.498-508.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Poolman B., Hellingwerf K. J., Konings W. N. Regulation of the glutamate-glutamine transport system by intracellular pH in Streptococcus lactis. J Bacteriol. 1987 May;169(5):2272–2276. doi: 10.1128/jb.169.5.2272-2276.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Poolman B., Konings W. N. Relation of growth of Streptococcus lactis and Streptococcus cremoris to amino acid transport. J Bacteriol. 1988 Feb;170(2):700–707. doi: 10.1128/jb.170.2.700-707.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Poolman B., Nijssen R. M., Konings W. N. Dependence of Streptococcus lactis phosphate transport on internal phosphate concentration and internal pH. J Bacteriol. 1987 Dec;169(12):5373–5378. doi: 10.1128/jb.169.12.5373-5378.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Reid J. R., Coolbear T., Pillidge C. J., Pritchard G. G. Specificity of hydrolysis of bovine kappa-casein by cell envelope-associated proteinases from Lactococcus lactis strains. Appl Environ Microbiol. 1994 Mar;60(3):801–806. doi: 10.1128/aem.60.3.801-806.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Smid E. J., Driessen A. J., Konings W. N. Mechanism and energetics of dipeptide transport in membrane vesicles of Lactococcus lactis. J Bacteriol. 1989 Jan;171(1):292–298. doi: 10.1128/jb.171.1.292-298.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Smid E. J., Plapp R., Konings W. N. Peptide uptake is essential for growth of Lactococcus lactis on the milk protein casein. J Bacteriol. 1989 Nov;171(11):6135–6140. doi: 10.1128/jb.171.11.6135-6140.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Terzaghi B. E., Sandine W. E. Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol. 1975 Jun;29(6):807–813. doi: 10.1128/am.29.6.807-813.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Thompson J., Chassy B. M. Novel phosphoenolpyruvate-dependent futile cycle in Streptococcus lactis: 2-deoxy-D-glucose uncouples energy production from growth. J Bacteriol. 1982 Sep;151(3):1454–1465. doi: 10.1128/jb.151.3.1454-1465.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Tynkkynen S., Buist G., Kunji E., Kok J., Poolman B., Venema G., Haandrikman A. Genetic and biochemical characterization of the oligopeptide transport system of Lactococcus lactis. J Bacteriol. 1993 Dec;175(23):7523–7532. doi: 10.1128/jb.175.23.7523-7532.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES