1887

Abstract

In this report we examine the PEP-dependent phosphotransferase systems (PTSs) of EGD-e, especially those involved in glucose and cellobiose transport. This strain possesses in total 86 genes, encoding 29 complete PTSs for the transport of carbohydrates and sugar alcohols, and several single PTS components, possibly supporting transport of these compounds. By a systematic deletion analysis we identified the major PTSs involved in glucose, mannose and cellobiose transport, when grows in a defined minimal medium in the presence of these carbohydrates. Whereas all four PTS permeases belonging to the PTS family may be involved in mannose transport, only two of these (PTS-2 and PTS-3), and in addition at least one (PTS-1) of the five PTS permeases belonging to the PTS family, are able to transport glucose, albeit with different efficiencies. Cellobiose is transported mainly by one (PTS-4) of the six members belonging to the PTS family. In addition, PTS-1 appears to be also able to transport cellobiose. The transcription of the operons encoding PTS-2 and PTS-4 (but not that of the operon for PTS-3) is regulated by LevR-homologous PTS regulation domain (PRD) activators. Whereas the growth rate of the mutant lacking PTS-2, PTS-3 and PTS-1 is drastically reduced (compared with the wild-type strain) in the presence of glucose, and that of the mutant lacking PTS-4 and PTS-1 in the presence of cellobiose, replication of both mutants within epithelial cells or macrophages is as efficient as that of the wild-type strain.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.034934-0
2010-04-01
2019-10-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/156/4/1069.html?itemId=/content/journal/micro/10.1099/mic.0.034934-0&mimeType=html&fmt=ahah

References

  1. Arous, S., Buchrieser, C., Folio, P., Glaser, P., Namane, A., Hebraud, M. & Hechard, Y. ( 2004a; ). Global analysis of gene expression in an rpoN mutant of Listeria monocytogenes. Microbiology 150, 1581–1590.[CrossRef]
    [Google Scholar]
  2. Arous, S., Dalet, K. & Hechard, Y. ( 2004b; ). Involvement of the mpo operon in resistance to class IIa bacteriocins in Listeria monocytogenes. FEMS Microbiol Lett 238, 37–41.
    [Google Scholar]
  3. Barabote, R. D. & Saier, M. H., Jr ( 2005; ). Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69, 608–634.[CrossRef]
    [Google Scholar]
  4. Barrios, H., Valderrama, B. & Morett, E. ( 1999; ). Compilation and analysis of σ 54-dependent promoter sequences. Nucleic Acids Res 27, 4305–4313.[CrossRef]
    [Google Scholar]
  5. Blencke, H. M., Homuth, G., Ludwig, H., Mäder, U., Hecker, M. & Stülke, J. ( 2003; ). Transcriptional profiling of gene expression in response to glucose in Bacillus subtilis: regulation of the central metabolic pathways. Metab Eng 5, 133–149.[CrossRef]
    [Google Scholar]
  6. Brehm, K., Ripio, M. T., Kreft, J. & Vazquez-Boland, J. A. ( 1999; ). The bvr locus of Listeria monocytogenes mediates virulence gene repression by β-glucosides. J Bacteriol 181, 5024–5032.
    [Google Scholar]
  7. 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]
  8. Dalet, K., Arous, S., Cenatiempo, Y. & Hechard, Y. ( 2003; ). Characterization of a unique σ 54-dependent PTS operon of the lactose family in Listeria monocytogenes. Biochimie 85, 633–638.[CrossRef]
    [Google Scholar]
  9. Débarbouillé, M., Martin-Verstraete, I., Klier, A. & Rapoport, G. ( 1991; ). The transcriptional regulator LevR of Bacillus subtilis has domains homologous to both σ 54- and phosphotransferase system-dependent regulators. Proc Natl Acad Sci U S A 88, 2212–2216.[CrossRef]
    [Google Scholar]
  10. Deutscher, J. ( 2008; ). The mechanisms of carbon catabolite repression in bacteria. Curr Opin Microbiol 11, 87–93.[CrossRef]
    [Google Scholar]
  11. Deutscher, J., Francke, C. & Postma, P. W. ( 2006; ). How phosphotransferase system-related protein phosphorylation regulates carbohydrate metabolism in bacteria. Microbiol Mol Biol Rev 70, 939–1031.[CrossRef]
    [Google Scholar]
  12. Erni, B. ( 1989; ). Glucose transport in Escherichia coli. FEMS Microbiol Rev 5, 13–23.
    [Google Scholar]
  13. Eylert, E., Schär, J., Mertins, S., Stoll, R., Bacher, A., Goebel, W. & Eisenreich, W. ( 2008; ). Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol Microbiol 69, 1008–1017.[CrossRef]
    [Google Scholar]
  14. Glaser, P., Frangeul, L., Buchrieser, C., Rusniok, C., Amend, A., Baquero, F., Berche, P., Bloecker, H., Brandt, P. & other authors ( 2001; ). Comparative genomics of Listeria species. Science 294, 849–852.
    [Google Scholar]
  15. Götz, A. & Goebel, W. ( 2010; ). Glucose and glucose-6-phosphate as carbon sources in extra- and intracellular growth of enteroinvasive Escherichia coli and Salmonella enterica. Microbiology 156, in press
    [Google Scholar]
  16. Greenberg, D. B., Stülke, J. & Saier, M. H., Jr ( 2002; ). Domain analysis of transcriptional regulators bearing PTS regulatory domains. Res Microbiol 153, 519–526.[CrossRef]
    [Google Scholar]
  17. Joseph, B., Przybilla, K., Stühler, C., Schauer, K., Slaghuis, J., Fuchs, T. M. & Goebel, W. ( 2006; ). Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J Bacteriol 188, 556–568.[CrossRef]
    [Google Scholar]
  18. Joseph, B., Mertins, S., Stoll, R., Schar, J., Umesha, K. R., Luo, Q., Muller-Altrock, S. & Goebel, W. ( 2008; ). Glycerol-metabolism and PrfA activity in Listeria monocytogenes. J Bacteriol 190, 5412–5430.[CrossRef]
    [Google Scholar]
  19. Mertins, S., Joseph, B., Goetz, M., Ecke, R., Seidel, G., Sprehe, M., Hillen, W., Goebel, W. & Müller-Altrock, S. ( 2007; ). Interference of components of the phosphoenolpyruvate phosphotransferase system with the central virulence gene regulator PrfA of Listeria monocytogenes. J Bacteriol 189, 473–490.[CrossRef]
    [Google Scholar]
  20. Milenbachs-Lukowiak, A., Mueller, K. J., Freitag, N. E. & Youngman, P. ( 2004; ). Deregulation of Listeria monocytogenes virulence gene expression by two distinct and semi-independent pathways. Microbiology 150, 321–333.[CrossRef]
    [Google Scholar]
  21. Milohanic, E., Glaser, P., Coppée, J. Y., Frangeul, L., Vega, Y., Vázquez-Boland, J. A., Kunst, F., Cossart, P. & Buchrieser, C. ( 2003; ). Transcriptome analysis of Listeria monocytogenes identifies three groups of genes differently regulated by PrfA. Mol Microbiol 47, 1613–1625.[CrossRef]
    [Google Scholar]
  22. Morett, E. & Buck, M. ( 1989; ). In vivo studies on the interaction of RNA polymerase-σ 54 with the Klebsiella pneumoniae and Rhizobium meliloti nifH promoters. The role of NifA in the formation of an open promoter complex. J Mol Biol 210, 65–77.[CrossRef]
    [Google Scholar]
  23. Parker, C. & Hutkins, R. W. ( 1997; ). Listeria monocytogenes Scott A transports glucose by high-affinity and low-affinity glucose transport systems. Appl Environ Microbiol 63, 543–546.
    [Google Scholar]
  24. Postma, P. W., Lengeler, J. W. & Jacobson, G. R. ( 1993; ). Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57, 543–594.
    [Google Scholar]
  25. Premaratne, R. J., Lin, W. J. & Johnson, E. A. ( 1991; ). Development of an improved chemically defined minimal medium for Listeria monocytogenes. Appl Environ Microbiol 57, 3046–3048.
    [Google Scholar]
  26. Reizer, J., Bachem, S., Reizer, A., Arnaud, M., Saier, M. H., Jr & Stülke, J. ( 1999; ). Novel phosphotransferase system genes revealed by genome analysis – the complete complement of PTS proteins encoded within the genome of Bacillus subtilis. Microbiology 145, 3419–3429.
    [Google Scholar]
  27. Sambrook, J. & Russell, D. W. ( 2001; ). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  28. Stoll, R., Mertins, S., Joseph, B., Müller-Altrock, S. & Goebel, W. ( 2008; ). Modulation of PrfA activity in Listeria monocytogenes upon growth in different culture media. Microbiology 154, 3856–3876.[CrossRef]
    [Google Scholar]
  29. Studholme, D. J. & Dixon, R. ( 2003; ). Domain architectures of σ 54-dependent transcriptional activators. J Bacteriol 185, 1757–1767.[CrossRef]
    [Google Scholar]
  30. Stülke, J., Arnaud, M., Rapoport, 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]
  31. Sue, D., Fink, D., Wiedmann, M. & Boor, K. J. ( 2004; ). σ B-dependent gene induction and expression in Listeria monocytogenes during osmotic and acid stress conditions simulating the intestinal environment. Microbiology 150, 3843–3855.[CrossRef]
    [Google Scholar]
  32. van Tilbeurgh, H. & Declerck, N. ( 2001; ). Structural insights into the regulation of bacterial signalling proteins containing PRDs. Curr Opin Struct Biol 11, 685–693.[CrossRef]
    [Google Scholar]
  33. Wuenscher, M. D., Kohler, S., Goebel, W. & Chakraborty, T. ( 1991; ). Gene disruption by plasmid integration in Listeria monocytogenes: insertional inactivation of the listeriolysin determinant lisA. Mol Gen Genet 228, 177–182.
    [Google Scholar]
  34. Xue, J. & Miller, K. W. ( 2007; ). Regulation of the mpt operon in Listeria innocua by the ManR protein. Appl Environ Microbiol 73, 5648–5652.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.034934-0
Loading
/content/journal/micro/10.1099/mic.0.034934-0
Loading

Data & Media loading...

Supplements

[PDF](38 KB)

PDF

[PDF](115 KB)

PDF
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