1887

Abstract

transports glucose preferentially by a mannose-class phosphoenolpyruvate : sugar phosphotransferase system (PTS). The genomic analysis of allowed the authors to find a gene cluster () encoding the IIAB (), IIC () and IID () proteins of a mannose-class PTS, and a putative 121 aa protein of unknown function (encoded by ), homologues of which are also present in clusters that encode glucose/mannose transporters in other Gram-positive bacteria. The operon is constitutively expressed into a messenger, but an additional transcript was also detected. Upstream of the operon, two genes ( and ) were found which encode proteins resembling a transcriptional regulator and a membrane protein, respectively. Disruption of either or did not affect transcription, and had no effect on glucose uptake. Cells carrying a deletion transported glucose at a rate similar to that of the wild-type strain. By contrast, a disruption resulted in cells unable to transport glucose by the PTS, thus confirming the functional role of the genes. In addition, the mutant exhibited neither inducer exclusion of maltose nor glucose repression. This result confirms the need for glucose transport through the PTS to trigger these regulatory processes in .

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.28293-0
2006-01-01
2019-11-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/152/1/95.html?itemId=/content/journal/micro/10.1099/mic.0.28293-0&mimeType=html&fmt=ahah

References

  1. Abe, K. & Uchida, K. ( 1989; ). Correlation between depression of catabolite control of xylose metabolism and a defect in the phosphoenolpyruvate : mannose phosphotransferase system in Pediococcus halophilus. J Bacteriol 171, 1793–1800.
    [Google Scholar]
  2. Abranches, J., Chen, Y. Y. & Burne, R. A. ( 2003; ). Characterization of Streptococcus mutans strains deficient in EIIABMan of the sugar phosphotransferase system. Appl Environ Microbiol 69, 4760–4769.[CrossRef]
    [Google Scholar]
  3. Asanuma, N., Yoshii, T. & Hino, T. ( 2004; ). Molecular characteristics of phosphoenolpyruvate : mannose phosphotransferase system in Streptococcus bovis. Curr Microbiol 49, 4–9.
    [Google Scholar]
  4. Charrier, V., Deutscher, J., Galinier, A. & Martin-Verstraete, I. ( 1997; ). Protein phosphorylation chain of a Bacillus subtilis fructose-specific phosphotransferase system and its participation in regulation of the expression of the lev operon. Biochemistry 36, 1163–1172.[CrossRef]
    [Google Scholar]
  5. Chassy, B. M. & Thompson, J. ( 1983a; ). Regulation of lactose-phosphoenolpyruvate-dependent phosphotransferase system and β-d-phosphogalactoside galactohydrolase activities in Lactobacillus casei. J Bacteriol 154, 1195–1203.
    [Google Scholar]
  6. Chassy, B. M. & Thompson, J. ( 1983b; ). Regulation and characterization of the galactose-phosphoenolpyruvate-dependent phosphotransferase system in Lactobacillus casei. J Bacteriol 154, 1204–1214.
    [Google Scholar]
  7. Cochu, A., Vadeboncoeur, C., Moineau, S. & Frenette, M. ( 2003; ). Genetic and biochemical characterization of the phosphoenolpyruvate : glucose/mannose phosphotransferase system of Streptococcus thermophilus. Appl Environ Microbiol 69, 5423–5432.[CrossRef]
    [Google Scholar]
  8. Dalet, K., Cenatiempo, Y., Cossart, P. & Hechard, Y. ( 2001; ). A σ 54-dependent PTS permease of the mannose family is responsible for sensitivity of Listeria monocytogenes to mesentericin Y105. Microbiology 147, 3263–3269.
    [Google Scholar]
  9. Deutscher, J., Kessler, U., Alpert, C. A. & Hengstenberg, W. ( 1984; ). Bacterial phosphoenolpyruvate-dependent phosphotransferase system – P-Ser-HPr and its possible regulatory function. Biochemistry 23, 4455–4460.[CrossRef]
    [Google Scholar]
  10. Deutscher, J., Küster, E., Bergstedt, U., Charrier, V. & Hillen, W. ( 1995; ). Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in Gram-positive bacteria. Mol Microbiol 15, 1049–1053.[CrossRef]
    [Google Scholar]
  11. Deutscher, J., Galinier, A. & Martin-Verstraete, I. ( 2002; ). Carbohydrate uptake and metabolism. In Bacillus subtilis and its Closest Relatives: from Genes to Cells, pp. 129–150. Edited by L. Sonenshein, J. Hoch & R. Losick. Washington, DC: American Society for Microbiology.
  12. Djordjevic, G. M., Tchieu, J. H. & Saier, M. H., Jr ( 2001; ). Genes involved in control of galactose uptake in Lactobacillus brevis and reconstitution of the regulatory system in Bacillus subtilis. J Bacteriol 183, 3224–3236.[CrossRef]
    [Google Scholar]
  13. Dossonnet, V., Monedero, V., Zagorec, M., Galinier, A., Pérez-Martínez, G. & Deutscher, J. ( 2000; ). Phosphorylation of HPr by the bifunctional HPr kinase/P-Ser-HPr phosphatase from Lactobacillus casei controls catabolite repression and inducer exclusion but not inducer expulsion. J Bacteriol 182, 2582–2590.[CrossRef]
    [Google Scholar]
  14. Erni, B., Zanolari, B., Graff, P. & Kocher, H. P. ( 1989; ). Mannose permease of Escherichia coli. Domain structure and function of the phosphorylating subunit. J Biol Chem 264, 18733–18741.
    [Google Scholar]
  15. Galinier, A., Kravanja, M., Engelmann, R., Hengstenberg, W., Kilhoffer, M. C., Deutscher, J. & Haiech, J. ( 1998; ). New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc Natl Acad Sci U S A 95, 1823–1828.[CrossRef]
    [Google Scholar]
  16. Gauthier, L., Thomas, S., Gagnon, G., Frenette, M., Trahan, L. & Vadeboncoeur, C. ( 1994; ). Positive selection for resistance to 2-deoxyglucose gives rise, in Streptococcus salivarius, to seven classes of pleiotropic mutants, including ptsH and ptsI missense mutants. Mol Microbiol 13, 1101–1109.[CrossRef]
    [Google Scholar]
  17. Héchard, Y., Pelletier, C., Cenatiempo, Y. & Frère, J. ( 2001; ). Analysis of σ 54-dependent genes in Enterococcus faecalis: a mannose PTS permease (EIIMan) is involved in sensitivity to a bacteriocin, mesentericin Y105. Microbiology 147, 1575–1580.
    [Google Scholar]
  18. Klaenhammer, T., Altermann, E., Arigoni, F. & 33 other authors ( 2002; ). Discovering lactic acid bacteria by genomics. Antonie van Leeuwenhoek 82, 29–58.[CrossRef]
    [Google Scholar]
  19. Kravanja, M., Engelmann, R., Dossonnet, V. & 7 other authors ( 1999; ). The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: the HPr kinase/phosphatase. Mol Microbiol 31, 59–66.[CrossRef]
    [Google Scholar]
  20. Lapointe, R., Frenette, M. & Vadeboncoeur, C. ( 1993; ). Altered expression of several genes in IIIL Man-defective mutants of Streptococcus salivarius demonstrated by two-dimensional gel electrophoresis of cytoplasmic proteins. Res Microbiol 144, 305–316.[CrossRef]
    [Google Scholar]
  21. Leloup, L., Ehrlich, S. D., Zagorec, M. & Morel-Deville, F. ( 1997; ). Single-crossover integration in the Lactobacillus sake chromosome and insertional inactivation of the ptsI and lacL genes. Appl Environ Microbiol 63, 2117–2123.
    [Google Scholar]
  22. Lortie, L.-A., Pelletier, M., Vadeboncoeur, C. & Frenette, M. ( 2000; ). The gene encoding IIABL Man in Streptococcus salivarius is part of a tetracistronic operon encoding a phosphoenolpyruvate : mannose/glucose phosphotransferase system. Microbiology 146, 677–685.
    [Google Scholar]
  23. Mazé, A., Boël, G., Poncet, S., Mijakovic, I., Breton, Y. L., Benachour, A., Monedero, V., Deutscher, J. & Hartke, A. ( 2004; ). The Lactobacillus casei ptsHI47T mutation leads to overexpression of a LevR-regulated, but RpoN-independent operon encoding a mannose class phosphotransferase system. J Bacteriol 186, 4543–4555.[CrossRef]
    [Google Scholar]
  24. Monedero, V., Kuipers, O. P., Jamet, E. & Deutscher, J. ( 2001; ). Regulatory functions of serine-46-phosphorylated HPr in Lactococcus lactis. J Bacteriol 183, 3391–3398.[CrossRef]
    [Google Scholar]
  25. Posno, M., Leer, R. J., van Luijk, N., van Giezen, M. J. F., Heuvelmans, P. T., Lokman, B. C. & Pouwels, P. H. ( 1991; ). Incompatibility of Lactobacillus vectors with replicons derived from small cryptic Lactobacillus plasmids and segregational instability of the introduced vectors. Appl Environ Microbiol 57, 1822–1828.
    [Google Scholar]
  26. Postma, P. W., Lengeler, J. W. & Jacobson, G. R. ( 1993; ). Phosphoenolpyruvate : carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57, 543–594.
    [Google Scholar]
  27. Ramnath, M., Arous, S., Gravesen, A., Hastings, J. W. & Hechard, Y. ( 2004; ). Expression of mptC of Listeria monocytogenes induces sensitivity to class IIa bacteriocins in Lactococcus lactis. Microbiology 150, 2663–2668.[CrossRef]
    [Google Scholar]
  28. Reizer, J., Hoischen, C., Titgemeyer, F. & 7 other authors ( 1998; ). A novel protein kinase that controls carbon catabolite repression in bacteria. Mol Microbiol 27, 1157–1169.[CrossRef]
    [Google Scholar]
  29. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  30. Schumacher, M. A., Allen, G. S., Diel, M., Seidel, G., Hillen, W. & Brennan, R. G. ( 2004; ). Structural basis for allosteric control of the transcription regulator CcpA by the phosphoprotein HPr-Ser46-P. Cell 118, 731–741.[CrossRef]
    [Google Scholar]
  31. Stülke, J., Arnaud, M., Rapaport, G. & Martin-Verstraete, I. ( 1998; ). PRD – a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria. Mol Microbiol 28, 865–874.[CrossRef]
    [Google Scholar]
  32. Thompson, J. & Chassy, B. M. ( 1985; ). Intracellular phosphorylation of glucose analogs via the phosphoenolpyruvate : mannose-phosphotransferase system in Streptococcus lactis. J Bacteriol 162, 224–234.
    [Google Scholar]
  33. Titgemeyer, F. & Hillen, W. ( 2002; ). Global control of sugar metabolism: a Gram-positive solution. Antonie Van Leeuwenhoek 82, 59–71.[CrossRef]
    [Google Scholar]
  34. Vadeboncoeur, C. & Pelletier, M. ( 1997; ). The phosphoenolpyruvate : sugar phosphotransferase system of oral streptococci and its role in the control of sugar metabolism. FEMS Microbiol Rev 19, 187–207.[CrossRef]
    [Google Scholar]
  35. Veyrat, A., Monedero, V. & Pérez-Martínez, G. ( 1994; ). Glucose transport by the phosphoenolpyruvate : mannose phosphotransferase system in Lactobacillus casei ATCC 393 and its role in carbon catabolite repression. Microbiology 140, 1141–1149.[CrossRef]
    [Google Scholar]
  36. Viana, R., Monedero, V., Dossonnet, V., Vadeboncoeur, C., Pérez-Martínez, G. & Deutscher, J. ( 2000; ). Enzyme I and HPr from Lactobacillus casei: their role in sugar transport, carbon catabolite repression and inducer exclusion. Mol Microbiol 36, 570–584.
    [Google Scholar]
  37. Yebra, M. J., Veyrat, A., Santos, M. A. & Pérez-Martínez, G. ( 2000; ). Genetics of l-sorbose transport and metabolism in Lactobacillus casei. J Bacteriol 182, 155–163.[CrossRef]
    [Google Scholar]
  38. Yebra, M. J., Viana, R., Monedero, V., Deutscher, J. & Pérez-Martínez, G. ( 2004; ). An esterase gene from Lactobacillus casei cotranscribed with genes encoding a phosphoenolpyruvate : sugar phosphotransferase system and regulated by a LevR-like activator and σ 54 factor. J Mol Microbiol Biotechnol 8, 117–128.[CrossRef]
    [Google Scholar]
  39. Zúñiga, M., Comas, I., Linaje, R., Monedero, V., Yebra, M. J., Esteban, C. D., Deutscher, J., Pérez-Martínez, G. & González-Candelas, F. ( 2005; ). Horizontal gene transfer in the molecular evolution of mannose PTS transporters. Mol Biol Evol 22, 1673–1685.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.28293-0
Loading
/content/journal/micro/10.1099/mic.0.28293-0
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