1887

Microbiology Society logo

Volume 146, Issue 3

The gene encoding IIAB in is part of a tetracistronic operon encoding a phosphoenolpyruvate:mannose/glucose phosphotransferase system

The GenBank accession number for the sequence reported in this paper is AF130465.

Free

Abstract

Glucose and mannose are transported in streptococci by the mannose-PTS (phosphoenolpyruvate:mannose phosphotransferase system), which consists of a cytoplasmic IIAB protein, called IIAB, and an uncharacterized membrane permease. This paper reports the characterization of the operon encoding the specific components of the mannose-PTS of . The operon was composed of four genes, , , and . These genes were transcribed from a canonical promoter () into a 36 kb polycistronic mRNA that contained a 5′-UTR (untranslated region). The predicted gene product encoded a 355 kDa protein and contained the amino acid sequences of the IIA and IIB phosphorylation sites already determined from purified . Expression of in generated a 35 kDa protein that reacted with antibodies. The predicted ManM protein had an estimated size of 272 kDa. ManM had similarity with IIC domains of the mannose-EII family, but did not possess the signature proposed for mannose-IIC proteins from Gram-negative bacteria. From multiple alignment analyses of sequences available in current databases, the following modified IIC signature is proposed: GXG[DNH]XG[LIVM]XG[STL][LT][EQ]. The deduced product of was a hydrophobic protein with a predicted molecular mass of 334 kDa. The ManN protein contained an amino acid sequence similar to the signature sequence of the IID domains of the mannose-EII family. encoded a 137 kDa protein. This gene was also transcribed as a monocistronic mRNA from a promoter located in the intergenic region. A search of current databases revealed the presence of , ManM, ManN and ManO orthologues in , , and . This work has elucidated the molecular structure of the mannose PTS in streptococci and enterococci, and demonstrated the presence of a putative regulatory protein (ManO) within the operon.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): enzyme II , man operon , PEP, phosphoenolpyruvate , phosphotransferase system , PTS, phosphotransferase system and streptococci
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-146-3-677
2000-03-01
2023-03-27
Loading full text...

Full text loading...

/deliver/fulltext/micro/146/3/1460677a.html?itemId=/content/journal/micro/10.1099/00221287-146-3-677&mimeType=html&fmt=ahah

References

  1. Ausubel F. A., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A., Struhl K.editors 1990 Current Protocols in Molecular Biology New York: Greene Publishing/Wiley-Interscience;
     [Google Scholar]
  2. Bouma C. L., Roseman S. 1996; Sugar transport by the marine chitinolytic bacterium Vibrio furnissii. Molecular cloning and analysis of the mannose/glucose permease. J Biol Chem 271:33468–33475 [CrossRef]
     [Google Scholar]
  3. Bourassa S., Vadeboncoeur C. 1992; Expression of an inducible enzyme II fructose and activation of a cryptic enzyme II glucose in glucose-grown cells of spontaneous mutants of Streptococcus salivarius lacking the low-molecular-mass form of IIIMan, a component of the phosphoenolpyruvate:mannose phosphotransferase system. J Gen Microbiol 138:769–777 [CrossRef]
     [Google Scholar]
  4. Bourassa S., Gauthier L., Giguère R., Vadeboncoeur C. 1990; A IIIMan protein is involved in the transport of glucose, mannose and fructose by oral streptococci. Oral Microbiol Immunol 5:288–297
     [Google Scholar]
  5. Brochu D., Trahan L., Jacques M., Lavoie M. L., Frenette M., Vadeboncoeur C. 1993; Alterations in the cellular envelope of spontaneous -defective mutants of Streptococcus salivarius. J Gen Microbiol 139:1291–1300 [CrossRef]
     [Google Scholar]
  6. Chen J. D., Morrison D. A. 1987; Cloning of Streptococcus pneumoniae DNA fragments in Escherichia coli requires vectors protected by strong transcriptional terminators. Gene 55:179–187 [CrossRef]
     [Google Scholar]
  7. Chen Y. Y., Hall T. H., Burne R. A. 1998; Streptococcus salivarius urease expression: involvement of the phosphoenolpyruvate:sugar phosphotransferase system. FEMS Microbiol Lett 165:117–122 [CrossRef]
     [Google Scholar]
  8. Coburn G. A., Mackie G. A. 1999; Degradation of mRNA in Escherichia coli: an old problem with some new twists. Prog Nucleic Acid Res Mol Biol 62:55–108
     [Google Scholar]
  9. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395 [CrossRef]
     [Google Scholar]
  10. Dillard J. P., Yother J. 1991; Analysis of Streptococcus pneumoniae sequences cloned into Escherichia coli: effect of promoter strength and transcription terminators. J Bacteriol 173:5105–5109
     [Google Scholar]
  11. Erni B., Zanolari B., Kocher H. P. 1987; The mannose permease of Escherichia coli consists of three different proteins. Amino acid sequence and function in sugar transport, sugar phosphorylation, and penetration of phage lambda DNA. J Biol Chem 262:5238–5247
     [Google Scholar]
  12. Fang L., Hou Y., Inouye M. 1998; Role of the cold-box region in the 5′-untranslated region of the cspA mRNA in its transient expression at low temperature in Escherichia coli. J Bacteriol 180:90–95
     [Google Scholar]
  13. Farrow J. A. E., Collins M. D. 1984; DNA base composition, DNA–DNA homology and long chain fatty acid studies on Streptococcus thermophilus and Streptococcus salivarius. J Gen Microbiol 130:357–362
     [Google Scholar]
  14. Gagnon G., Vadeboncoeur C., Gauthier L., Frenette M. 1995; Regulation of ptsH and ptsI gene expression in Streptococcus salivarius ATCC 25975. Mol Microbiol 16:1111–1121 [CrossRef]
     [Google Scholar]
  15. Gauthier L., Bourassa S., Brochu D., Vadeboncoeur C. 1990; Control of sugar utilization in oral streptococci. Properties of phenotypically distinct 2-deoxyglucose-resistant mutants of Streptococcus salivarius. Oral Microbiol Immunol 5:352–359 [CrossRef]
     [Google Scholar]
  16. Gutknecht R., Lanz R., Erni B. 1998; Mutational analysis of invariant arginines in the IIABMan subunit of the Escherichia coli phosphotransferase system. J Biol Chem 273:12234–12238 [CrossRef]
     [Google Scholar]
  17. Huber F., Erni B. 1996; Membrane topology of the mannose transporter of Escherichia coli K12. Eur J Biochem 239:810–817 [CrossRef]
     [Google Scholar]
  18. Kushner S. R. 1996; mRNA decay. In Escherichia coli and Salmonella typhimurium: Cellular and Molecular Biology pp. 849–860Edited by Neidhart F. C.others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  19. Jacobson G. R., Saraceni-Richards C. 1993; The Escherichia coli mannitol permease as a model for transport via the bacterial phosphotransferase system. J Bioenerg Biomembr 25:621–626
     [Google Scholar]
  20. Jiang W., Fang L., Inouye M. 1996; The role of the 5′-end untranslated region of the mRNA for CspA, the major cold-shock protein of Escherichia coli, in cold-shock adaptation. J Bacteriol 178:4919–4925
     [Google Scholar]
  21. Lapointe R., Frenette M., Vadeboncoeur C. 1993; Altered expression of several genes in -defective mutants of Streptococcus salivarius demonstrated by two-dimensional gel electrophoresis of cytoplasmic proteins. Res Microbiol 144:305–316 [CrossRef]
     [Google Scholar]
  22. Lengeler J. W., Jahreis K., Wehmeier U. F. 1994; Enzymes II of the phosphoenol pyruvate-dependent phosphotransferase systems: their structure and function in carbohydrate transport. Biochim Biophys Acta 1188:1–28 [CrossRef]
     [Google Scholar]
  23. Lisser S., Margalit H. 1993; Compilation of E. coli mRNA promoter sequences. Nucleic Acids Res 21:1507–1516 [CrossRef]
     [Google Scholar]
  24. Lortie L. A., Gagnon G., Frenette M. 1994; IS1139 from Streptococcus salivarius: identification and characterization of an insertion sequence-like element related to mobile DNA elements from Gram-negative bacteria. Plasmid 32:1–9 [CrossRef]
     [Google Scholar]
  25. Marsh P., Martin M. 1992 Oral Microbiology, 3rd edn. pp. 26–47 London: Chapman & Hall;
     [Google Scholar]
  26. Martin B., Alloing G., Boucraut C., Claverys J. P. 1989; The difficulty of cloning Streptococcus pneumoniae mal and ami loci in Escherichia coli: toxicity of malX and amiA gene products. Gene 80:227–238 [CrossRef]
     [Google Scholar]
  27. Martin-Verstraete I., Debarbouille M., Klier A., Rapoport G. 1990; Levanase operon of Bacillus subtilis includes a fructose-specific phosphotransferase system regulating the expression of the operon. J Mol Biol 214:657–671 [CrossRef]
     [Google Scholar]
  28. Moran C. P. Jr, Lang N., LeGrice S. F., Lee G., Stephens M., Sonenshein A. L., Pero J., Losick R. 1982; Nucleotide sequences that signal the initiation of transcription and translation in Bacillus subtilis. Mol Gen Genet 186:339–346 [CrossRef]
     [Google Scholar]
  29. Nierlich D. P., Murakawa G. J. 1996; The decay of bacterial messenger RNA. Prog Nucleic Acid Res Mol Biol 52:153–216
     [Google Scholar]
  30. Nunn R. S., Markovic-Housley Z., Génovésio-Taverne J.-C., Flükiger K., Rizkallah P. J., Jansonius J. N., Schirmer T., Erni B. 1996; Structure of the IIA domain of the mannose transporter from Escherichia coli at 1·7 Å resolution. J Mol Biol 259:502–511 [CrossRef]
     [Google Scholar]
  31. Pelletier M., Frenette M., Vadeboncoeur C. 1995; Distribution of proteins similar to and of the Streptococcus salivarius phosphoenolpyruvate:mannose-glucose phosphotransferase system among oral and nonoral bacteria. J Bacteriol 177:2270–2275
     [Google Scholar]
  32. Pelletier M., Lortie L.-A., Frenette M., Vadeboncoeur C. 1998; The phosphoenolpyruvate:mannose phosphotransferase system of Streptococcus salivarius. Functional and biochemical characterization of and . Biochemistry 37:1604–1612 [CrossRef]
     [Google Scholar]
  33. Postma P. W., Lengeler J. W., Jacobson G. R. 1993; Phosphoenolpyruvate:carbohydrate phosphotransferase systems of bacteria. Microbiol Rev 57:543–594
     [Google Scholar]
  34. Postma P. W., Lengeler J. W., Jacobson G. R. 1996; Phosphoenolpyruvate:carbohydrate phosphotransferase systems. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp. 1149–1174Edited by Neidhart F. C.others Washington, DC: American Society for Microbiology;
     [Google Scholar]
  35. Reizer J., Ramseier T. M., Reizer A., Charbit A., Saier M. H. Jr 1996; Novel phosphotransferase genes revealed by bacterial genome sequencing: a gene cluster encoding a putative N-acetylgalactosamine metabolic pathway in Escherichia coli. Microbiology 142:231–250 [CrossRef]
     [Google Scholar]
  36. Rhiel E., Flukiger K., Wehrli C., Erni B. 1994; The mannose transporter of Escherichia coli K12, oligomeric structure, and function of two conserved cysteines. Biol Chem Hoppe Seyler 375:551–559 [CrossRef]
     [Google Scholar]
  37. Saier M. H. Jr, Reizer J. 1992; Proposed uniform nomenclature for the proteins and protein domains of the bacterial phosphoenolpyruvate:sugar phosphotransferase system. J Bacteriol 174:1433–1438
     [Google Scholar]
  38. Stassi D. L., Lacks S. A. 1982; Effect of strong promoters on the cloning in Escherichia coli of DNA fragments from Streptococcus pneumoniae. Gene 18:319–328 [CrossRef]
     [Google Scholar]
  39. Szoke P. A., Allen T. L., deHaseth P. L. 1987; Promoter recognition by Escherichia coli RNA polymerase: effects of base substitutions in the −10 and −35 regions. Biochemistry 26:6188–6194 [CrossRef]
     [Google Scholar]
  40. Vadeboncoeur C. 1984; Structure and properties of the phosphoenolpyruvate:glucose phosphotransferase system of oral streptococci. Can J Microbiol 30:495–502 [CrossRef]
     [Google Scholar]
  41. 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]
  42. Veyrat A., Gosalbes M. J., Perez-Martinez G. 1996; Lactobacillus curvatus has a glucose transport system homologous to the mannose family of phosphoenolpyruvate-dependent phosphotransferase systems. Microbiology 142:3469–3477 [CrossRef]
     [Google Scholar]
  43. Waterfield N. R., Le Page R. W., Wilson P. W., Wells J. M. 1995; The isolation of lactococcal promoters and their use in investigating bacterial luciferase synthesis in Lactococcus lactis. Gene 165:9–15 [CrossRef]
     [Google Scholar]
  44. Wehmeier U. F., Lengeler J. W. 1994; Sequence of the sor-operon for l-sorbose utilization from Klebsiella pneumoniae KAY2026. Biochim Biophys Acta 1208:348–351 [CrossRef]
     [Google Scholar]
  45. Wouters J. A., Sanders J.-W., Kok J., de Vos W. M., Kuipers O. P., Abee T. 1998; Clustered organization and transcriptional analysis of a family of five csp genes of Lactococcus lactis MG1363. Microbiology 144:2885–2893 [CrossRef]
     [Google Scholar]
  46. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-146-3-677
Loading
The gene encoding IIABLMan in Streptococcus salivarius is part of a tetracistronic operon encoding a phosphoenolpyruvate:mannose/glucose phosphotransferase systemThe GenBank accession number for the sequence reported in this paper is AF130465.
Microbiology 146, 677 (2000); https://doi.org/10.1099/00221287-146-3-677
/content/journal/micro/10.1099/00221287-146-3-677
/content/journal/micro/10.1099/00221287-146-3-677
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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