1887

Abstract

is known to take up extracellular peptides via at least three distinct peptide transporters. The well-described oligopeptide transporter Opp alone is able to ensure the growth of in milk, while the di- and tripeptide transporter DtpT is involved in a peptide-dependent signalling mechanism. The oligopeptide Opt transporter displays two peptide-binding proteins, OptA and OptS. We previously demonstrated that OptA-dependent transport is dedicated to nutritional peptides, as an mutant (of a strain devoid of Opp) has an impaired capacity to grow in milk. Using isogenic peptide transport mutants, this study shows that biosynthesis of the Opt transporter is much less sensitive to downregulation that is dependent on extracellular peptides taken up by DtpT than is Opp biosynthesis; this peptide-dependent regulation relies on the transcriptional repressor CodY. We demonstrate the dual function of the Opt system; while OptA contributes to the bacterial nutrition during growth in milk, OptS is involved in the transport of signalling peptides derived from milk and controlling expression. So, these results shed new light on the peptide-dependent regulation relying on two peptide transporters with different specificities: DtpT and Opt (via OptS).

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.048173-0
2011-06-01
2020-01-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/6/1612.html?itemId=/content/journal/micro/10.1099/mic.0.048173-0&mimeType=html&fmt=ahah

References

  1. Atlan D., Laloi P., Portalier R.. ( 1989;). Isolation and characterization of aminopeptidase-deficent Lactobacillus bulgaricus mutants. Appl Environ Microbiol55:1717–1723[PubMed]
    [Google Scholar]
  2. Birnboim H. C., Doly J.. ( 1979;). A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res7:1513–1523 [CrossRef][PubMed]
    [Google Scholar]
  3. Biswas I., Gruss A., Ehrlich S. D., Maguin E.. ( 1993;). High-efficiency gene inactivation and replacement system for Gram-positive bacteria. J Bacteriol175:3628–3635[PubMed]
    [Google Scholar]
  4. Bolotin A., Wincker P., Mauger S., Jaillon O., Malarme K., Weissenbach J., Ehrlich S. D., Sorokin A.. ( 2001;). The complete genome sequence of the lactic acid bacterium Lactococcus lactis ssp. lactis IL1403. Genome Res11:731–753 [CrossRef][PubMed]
    [Google Scholar]
  5. Bradford M. M.. ( 1976;). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72:248–254 [CrossRef][PubMed]
    [Google Scholar]
  6. Brøndsted L., Hammer K.. ( 1999;). Use of the integration elements encoded by the temperate lactococcal bacteriophage TP901-1 to obtain chromosomal single-copy transcriptional fusions in Lactococcus lactis . Appl Environ Microbiol65:2859–2865
    [Google Scholar]
  7. Charbonnel P., Lamarque M., Piard J. C., Gilbert C., Juillard V., Atlan D.. ( 2003;). Diversity of oligopeptide transport specificity in Lactococcus lactis species. A tool to unravel the role of OppA in uptake specificity. J Biol Chem278:14832–14840 [CrossRef][PubMed]
    [Google Scholar]
  8. den Hengst C. D., van Hijum S. A., Geurts J. M., Nauta A., Kok J., Kuipers O. P.. ( 2005;). The Lactococcus lactis CodY regulon: identification of a conserved cis-regulatory element. J Biol Chem280:34332–34342 [CrossRef][PubMed]
    [Google Scholar]
  9. Detmers F. J., Lanfermeijer F. C., Abele R., Jack R. W., Tampé R., Konings W. N., Poolman B.. ( 2000;). Combinatorial peptide libraries reveal the ligand-binding mechanism of the oligopeptide receptor OppA of Lactococcus lactis . Proc Natl Acad Sci U S A97:12487–12492 [CrossRef][PubMed]
    [Google Scholar]
  10. de Vos W. M., Vos P., de Haard H., Boerrigter I.. ( 1989;). Cloning and expression of the Lactococcus lactis subsp. cremoris SK11 gene encoding an extracellular serine proteinase. Gene85:169–176 [CrossRef][PubMed]
    [Google Scholar]
  11. Doeven M. K., Kok J., Poolman B.. ( 2005;). Specificity and selectivity determinants of peptide transport in Lactococcus lactis and other microorganisms. Mol Microbiol57:640–649 [CrossRef][PubMed]
    [Google Scholar]
  12. Dower W. J., Miller J. F., Ragsdale C. W.. ( 1988;). High efficiency transformation of E. coli by high voltage electroporation. Nucleic Acids Res16:6127–6145 [CrossRef][PubMed]
    [Google Scholar]
  13. Fang G., Konings W. N., Poolman B.. ( 2000;). Kinetics and substrate specificity of membrane-reconstituted peptide transporter DtpT of Lactococcus lactis . J Bacteriol182:2530–2535 [CrossRef][PubMed]
    [Google Scholar]
  14. Guédon E., Renault P., Ehrlich S. D., Delorme C.. ( 2001;). Transcriptional pattern of genes coding for the proteolytic system of Lactococcus lactis and evidence for coordinated regulation of key enzymes by peptide supply. J Bacteriol183:3614–3622 [CrossRef][PubMed]
    [Google Scholar]
  15. Guédon E., Sperandio B., Pons N., Ehrlich S. D., Renault P.. ( 2005;). Overall control of nitrogen metabolism in Lactococcus lactis by CodY, and possible models for CodY regulation in Firmicutes. Microbiology151:3895–3909 [CrossRef][PubMed]
    [Google Scholar]
  16. Juillard V., Le Bars D., Kunji E. R., Konings W. N., Gripon J. C., Richard J.. ( 1995;). Oligopeptides are the main source of nitrogen for Lactococcus lactis during growth in milk. Appl Environ Microbiol61:3024–3030[PubMed]
    [Google Scholar]
  17. Koide A., Perego M., Hoch J. A.. ( 1999;). ScoC regulates peptide transport and sporulation initiation in Bacillus subtilis . J Bacteriol181:4114–4117[PubMed]
    [Google Scholar]
  18. Kunji E. R., Smid E. J., Plapp R., Poolman B., Konings W. N.. ( 1993;). Di-tripeptides and oligopeptides are taken up via distinct transport mechanisms in Lactococcus lactis . J Bacteriol175:2052–2059[PubMed]
    [Google Scholar]
  19. Kunji E. R., Hagting A., De Vries C. J., Juillard V., Haandrikman A. J., Poolman B., Konings W. N.. ( 1995;). Transport of β-casein-derived peptides by the oligopeptide transport system is a crucial step in the proteolytic pathway of Lactococcus lactis . J Biol Chem270:1569–1574 [CrossRef][PubMed]
    [Google Scholar]
  20. Lamarque M., Charbonnel P., Aubel D., Piard J.-C., Atlan D., Juillard V.. ( 2004;). A multifunction ABC transporter (Opt) contributes to diversity of peptide uptake specificity within the genus Lactococcus . J Bacteriol186:6492–6500 [CrossRef][PubMed]
    [Google Scholar]
  21. Lazazzera B. A.. ( 2001;). The intracellular function of extracellular signaling peptides. Peptides22:1519–1527 [CrossRef][PubMed]
    [Google Scholar]
  22. Marugg J. D., Meijer W., van Kranenburg R., Laverman P., Bruinenberg P. G., de Vos W. M.. ( 1995;). Medium-dependent regulation of proteinase gene expression in Lactococcus lactis: control of transcription initiation by specific dipeptides. J Bacteriol177:2982–2989[PubMed]
    [Google Scholar]
  23. Miller J.. ( 1992;). A Short Course in Bacterial Genetics: a Laboratory Manual and Handbook for Escherichia coli and Related Bacteria Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press;
    [Google Scholar]
  24. Monnet V.. ( 2003;). Bacterial oligopeptide-binding proteins. Cell Mol Life Sci60:2100–2114 [CrossRef][PubMed]
    [Google Scholar]
  25. Peltoniemi K., Vesanto E., Palva A.. ( 2002;). Genetic characterization of an oligopeptide transport system from Lactobacillus delbrueckii subsp. bulgaricus . Arch Microbiol177:457–467 [CrossRef][PubMed]
    [Google Scholar]
  26. Poolman B., Konings W. N.. ( 1988;). Relation of growth of Streptococcus lactis and Streptococcus cremoris to amino acid transport. J Bacteriol170:700–707[PubMed]
    [Google Scholar]
  27. Sonenshein A. L.. ( 2005;). CodY, a global regulator of stationary phase and virulence in Gram-positive bacteria. Curr Opin Microbiol8:203–207 [CrossRef][PubMed]
    [Google Scholar]
  28. Terzaghi B. E., Sandine W. E.. ( 1975;). Improved medium for lactic streptococci and their bacteriophages. Appl Microbiol29:807–813[PubMed]
    [Google Scholar]
  29. Tynkkynen S., Buist G., Kunji E., Kok J., Poolman B., Venema G., Haandrikman A.. ( 1993;). Genetic and biochemical characterization of the oligopeptide transport system of Lactococcus lactis . J Bacteriol175:7523–7532[PubMed]
    [Google Scholar]
  30. Wells J. M., Wilson P. W., Le Page R. W.. ( 1993;). Improved cloning vectors and transformation procedure for Lactococcus lactis . J Appl Bacteriol74:629–636[PubMed][CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.048173-0
Loading
/content/journal/micro/10.1099/mic.0.048173-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error