Chapter 34 : Carbohydrate Catabolism: Pathways and Regulation

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The central pathways of carbon metabolism are conserved in virtually all organisms, but details of specific biosynthetic and degradative pathways vary considerably between bacteria, plants, and animals. In and other staphylococcal species, relatively few molecular details are known about carbohydrate utilization, biosynthetic pathways, and nutritional requirements. The limited knowledge on sugar utilization systems is especially surprising, because was the first gram-positive bacterium in which the phosphoenolpyruvate (PEP)-dependent carbohydrate phosphotransferase system (PTS) was described. The phosphoryl-transfer chain begins with enzyme I (EI) and PEP and proceeds via the phosphocarrier protein HPr to the EIIA and EIIB domains of the PTS permeases. The uptake of glucose, mannose, mannitol, glucosamine, -acetylglucosamine, sucrose, lactose, galactose, and β-glucosides is reported to be PTS-dependent. Glucose-6-phosphate, produced by a glucose kinase, enters the EMP pathway, the main glycolytic pathway in staphylococci. Utilization of lactose and galactose in relies on the PTS-dependent uptake and phosphorylation of the sugars, resulting in lactose-6-phosphate and galactose-6-phosphate, respectively. The system consists of an EIICB enzyme, encoded by , and EIIA, encoded by , which together form the mannitol-specific PTS permease. The sucrose PTS permease, analyzed in and encoded by , is composed of fused EIIBC domains. Maltose utilization in is dependent on an α-glucosidase or maltase, whose gene, , is the second gene of the operon. The availability of carbohydrates, especially of glucose, leads to regulatory processes often referred to as glucose effect or carbon catabolite repression.

Citation: Brückner R, Rosenstein R. 2006. Carbohydrate Catabolism: Pathways and Regulation, p 427-433. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch34

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Staphylococcus aureus
Staphylococcus xylosus
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Alternative lactose catabolic pathways in staphylococci. Transport of lactose and galactose and their catabolism are shown. In , lactose and galactose are transported by the PEP:carbohydrate PTS. Internalized lactose-6-phosphate is hydrolyzed by a phospho-β-galactosidase to galactose-6-phosphate and glucose. Galactose-6-phosphate is catabolized through the tagatose-6-phosphate pathway. This pathway most likely exists in staphylococci exhibiting lactose PTS activity. In , and probably other staphylococcal species that do not possess a lactose PTS, a permease is responsible for the transport of lactose. Galactose uptake has not been studied in these species. Nonphosphorylated lactose is hydrolyzed by a β-galactosidase to yield glucose and galactose. Galactose is likely catabolized through the Leloir pathway. Glucose-6-phosphate, produced by a glucose kinase, enters the EMP pathway, the main glycolytic pathway in staphylococci. Only the galactoside-specific genes and their encoded products are mentioned in the pathways. Abbreviations: CM, cytoplasmic membrane; EI, enzyme I; EIIA, lactose-specific enzyme IIA; EIICB, lactose-specific enzyme IICB; HPr, histidine-containing protein; β-Gal, β-galactosidase; P-β-Gal, phospho-β-galactosidase; G6P-Isomerase, galactose-6-phosphate isomerase; G1P-Uridyltransferase, galactose-1-phosphate uridyltransferase; T6P-Kinase, tagatose-6-phosphate kinase; T1,6DP-Aldolase, tagatose-1,6-diphosphate aldolase; UDP-Gal, UDP-galactose; UDPGlc, UDP-glucose; UDP-G4-Epimerase, UDP-galactose-4 epimerase; PEP, phosphoenolpyruvate; P, phosphate; DP, diphosphate.

Citation: Brückner R, Rosenstein R. 2006. Carbohydrate Catabolism: Pathways and Regulation, p 427-433. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch34
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Image of FIGURE 2

Glucose-mediated carbon catabolite repression by the catabolite control protein CcpA in staphylococci. The components involved in regulation are: CcpA, carbon catabolite control protein; GlkA, glucose kinase; GlcU, PTS-independent glucose uptake protein; HPr, general PTS phosphocarrier protein; HPrK, HPr kinase/P-HPr phosphorylase; GlcA/GlcB, glucose-specific PTS permeases; FDP, fructose-1,6-diphosphate. The general PTS protein EI, essential for the transport of all PTS sugars, is omitted for clarity. The thick arrow represents a gene that is subject to carbon catabolite repression by CcpA via (catabolite-responsive element) interaction. The position of the CcpA binding site in the promoter region is indicated. The double line marked with CM represents the cytoplasmic membrane. The fact that some proteins may only function as dimers or multimers is not depicted. ATCC 1228 has apparently only one glucose-specific PTS permease. Glucose may be internalized by PTS-dependent or -independent transport. The glycolytic intermediate FDP activates kinase activity of HPrK, which produces P-ser-HPr by ATP-dependent phosphorylation. P-ser-HPr acts as a corepressor for CcpA, enabling the regulator to bind specifically to sites. When P prevails over ATP and FDP, HPrK dephosphorylates P-ser-HPr.

Citation: Brückner R, Rosenstein R. 2006. Carbohydrate Catabolism: Pathways and Regulation, p 427-433. In Fischetti V, Novick R, Ferretti J, Portnoy D, Rood J (ed), Gram-Positive Pathogens, Second Edition. ASM Press, Washington, DC. doi: 10.1128/9781555816513.ch34
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1. Baba, T.,, F. Takeuchi,, M. Kuroda,, H. Yuzawa,, K. Aoki,, A. Oguchi,, Y. Nagai,, N. Iwama,, K. Asano,, T. Naimi,, H. Kuroda,, L. Cui,, K. Yamamoto,, and K. Hiramatsu. 2002. Genome and virulence determinants of high virulence community-acquired MRSA. Lancet 359:18191827.
2. Bassias, J.,, and R. Brückner. 1998. Regulation of lactose utilization genes in Staphylococcus xylosus. J. Bacteriol. 180:22732279.
3. Beyreuther, K.,, H. Raufuss,, O. Schrecker,, and W. Hengstenberg. 1977. The phosphoenolpyruvatedependent phosphotransferase system of Staphylococcus aureus. 1. Amino-acid sequence of the phosphocarrier protein HPr. Eur. J. Biochem. 75:275286.
4. Blumenthal, H. J., 1972. Glucose catabolism in staphylococci, p. 111135. In J. O. Cohen (ed.), The Staphylococci. Wiley Interscience, New York, N.Y.
5. Breidt, F., Jr.,, W. Hengstenberg,, U. Finkeldei,, and G. C. Stewart. 1987. Identification of the genes for the lactose-specific components of the phosphotransferase system in the lac operon of Staphylococcus aureus. J. Biol. Chem. 262:1644416449.
6. Breidt, F., Jr.,, and G. C. Stewart. 1986. Cloning and expression of the phospho-beta-galactosidase gene of Staphylococcus aureus in Escherichia coli. J. Bacteriol. 166:10611066.
7. Brückner, R. 1997. Gene replacement in Staphylococcus carnosus and Staphylococcus xylosus. FEMS Microbiol. Lett. 151:18.
8. Brückner, R.,, and F. Titgemeyer. 2002. Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol. Lett. 209:141148.
9. Brückner, R.,, E. Wagner,, and F. Götz. 1993. Characterization of a sucrase gene from Staphylococcus xylosus. J. Bacteriol. 175:851857.
10. Christiansen, I.,, and W. Hengstenberg. 1996. Cloning and sequencing of two genes from Staphylococcus carnosus coding for glucose-specific PTS and their expression in Escherichia coli K-12. Mol. Gen. Genet. 250:375379.
11. Christiansen, I.,, and W. Hengstenberg. 1999. Staphylococcal phosphoenolpyruvate-dependent phosphotransferase system—two highly similar glucose permeases in Staphylococcus carnosus with different glucoside specificity: protein engineering in vivo? Microbiology 145:28812889.
12. de Vos, W. M.,, and E. E. Vaughan. 1994. Genetics of lactose utilization in lactic acid bacteria. FEMS Microbiol. Rev. 15:217237.
13. Dossonnet, V.,, V. Monedero,, M. Zagorec,, A. Galinier,, G. Pérez-Martínez,, and J. Deutscher. 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. 182:25822590.
14. Egeter, O.,, and R. Brückner. 1996. Catabolite repression mediated by the catabolite control protein CcpA in Staphylococcus xylosus. Mol. Microbiol. 21:739749.
15. Egeter, O.,, and R. Brückner. 1995. Characterization of a genetic locus essential for maltose-maltotriose utilization in Staphylococcus xylosus. J. Bacteriol. 177:24082415.
16. Eisermann, R.,, R. Fischer,, U. Kessler,, A. Neubauer,, and W. Hengstenberg. 1991. Staphylococcal phosphoenolpyruvate-dependent phosphotransferase system. Purification and protein sequencing of the Staphylococcus carnosus histidine-containing protein, and cloning and DNA sequencing of the ptsH gene. Eur. J. Biochem. 197:914.
17. Fiegler, H.,, J. Bassias,, I. Jankovic,, and R. Brückner. 1999. Identification of a gene in Staphylococcus xylosus encoding a novel glucose uptake protein. J. Bacteriol. 181:49294936.
18. Fischer, R.,, R. Eisermann,, B. Reiche,, and W. Hengstenberg. 1989. Cloning, sequencing and overexpression of the mannitol-specific enzyme-III-encoding gene of Staphylococcus carnosus. Gene 82:249257.
19. Fischer, R.,, and W. Hengstenberg. 1992. Mannitolspecific enzyme II of the phosphoenolpyruvate-dependent phosphotransferase system of Staphylococcus carnosus. Eur. J. Biochem. 204:963969.
20. Galinier, A.,, M. Kravanja,, R. Engelmann,, W. Hengstenberg,, M. C. Kilhoffer,, J. Deutscher,, and J. Haiech. 1998. New protein kinase and protein phosphatase families mediate signal transduction in bacterial catabolite repression. Proc. Natl. Acad. Sci. USA 95:18231828.
21. Gallegos, M.-T.,, R. Schleif,, A. Bairoch,, K. Hofmann,, and J. L. Ramos. 1997. AraC/XylS family of transcriptional regulators. Microbiol. Mol. Biol. Rev. 61:393410.
22. Gering, M.,, and R. Brückner. 1996. Transcriptional regulation of the sucrase gene of Staphylococcus xylosus by the repressor ScrR. J. Bacteriol. 178:462469.
23. Hengstenberg, W.,, D. Kohlbrecher,, E. Witt,, R. Kruse,, I. Christiansen,, D. Peters,, R. Pogge von Strandmann,, P. Stadtler,, B. Koch,, and H. R. Kalbitzer. 1993. Structure and function of proteins of the phosphotransferase system and of 6-phospho-beta-glycosidases in gram-positive bacteria. FEMS Microbiol. Rev. 12:149163.
24. Henkin, T. M. 1996. The role of CcpA transcriptional regulator in carbon metabolism in Bacillus subtilis. FEMS Microbiol. Lett. 135:915.
25. Holden, M. T.,, E. J. Feil,, J. A. Lindsay,, S. J. Peacock,, N. P. Day,, M. C. Enright,, T. J. Foster,, C. E. Moore,, L. Hurst,, R. Atkin,, A. Barron,, N. Bason,, S. D. Bentley,, C. Chillingworth,, T. Chillingworth,, C. Churcher,, L. Clark,, C. Corton,, A. Cronin,, J. Doggett,, L. Dowd,, T. Feltwell,, Z. Hance,, B. Harris,, H. Hauser,, S. Holroyd,, K. Jagels,, K. D. James,, N. Lennard,, A. Line,, R. Mayes,, S. Moule,, K. Mungall,, D. Ormond,, M. A. Quail,, E. Rabbinowitsch,, K. Rutherford,, M. Sanders,, S. Sharp,, M. Simmonds,, K. Stevens,, S. Whitehead,, B. G. Barrell,, B. G. Spratt,, and J. Parkhill. 2004. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proc. Natl. Acad. Sci. USA 101:97869791.
26. Hueck, C. J.,, W. Hillen,, and M. H. Saier, Jr. 1994. Analysis of a cis-active sequence mediating catabolite repression in gram-positive bacteria. Res. Microbiol. 145:503518.
27. Huynh, P. L.,, I. Jankovic,, N. F. Schnell,, and R. Brückner. 2000. Characterization of an HPr kinase mutant of Staphylococcus xylosus. J. Bacteriol. 182:18951902.
28. Jankovic, I.,, and R. Brückner. 2002. Carbon catabolite repression by the catabolite control protein CcpA in Staphylococcus xylosus. J. Mol. Microbiol. Biotechnol. 4:309314.
29. Jankovic, I.,, O. Egeter,, and R. Brückner. 2001. Analysis of catabolite control protein A-dependent repression in Staphylococcus xylosus by a genomic reporter gene system. J. Bacteriol. 183:580586.
30. Jankovic, I.,, J. Meyer,, and R. Brückner,. 2003. Catabolite control protein CcpA-dependent glucose repression in Staphylococcus xylosus: efficient activation of CcpA by glucose transported independently from the phosphotransferase system, p. 141146. In P. Dürre, and B. Friedrich (ed.), Regulatory Networks in Prokaryotes. Horizon Scientific Press, Norfolk, Va.
31. Kloos, W. E.,, K.-H. Schleifer,, and F. Götz,. 1991. The genus Staphylococcus, p. 13691420. In A. Balows,, H. G. Trüper,, M. Dwarkin,, W. Harder,, and K. H. Schleifer (ed.), The Procaryotes. Springer Verlag, Heidelberg, Germany.
32. Knezevic, I.,, S. Bachem,, A. Sickmann,, H. E. Meyer,, J. Stülke,, and W. Hengstenberg. 2000. Regulation of the glucose-specific phosphotransferase system (PTS) of Staphylococcus carnosus by the antiterminator protein glcT. Microbiology 146:23332342.
33. Knobloch, J. K.,, M. Nedelmann,, K. Kiel,, K. Bartscht,, M. A. Horstkotte,, S. Dobinsky,, H. Rohde,, and D. Mack. 2003. Establishment of an arbitrary PCR for rapid identification of Tn917 insertion sites in Staphylococcus epidermidis: characterization of biofilm-negative and nonmucoid mutants. Appl. Environ. Microbiol. 69:58125818.
34. Kohlbrecher, D.,, R. Eisermann,, and W. Hengstenberg. 1992. Staphylococcal phophoenolpyruvate-dependent phosphotransferase system: molecular cloning and nucleotide sequence of the Staphylococcus carnosus ptsI gene and expression and complementation studies of the gene product. J. Bacteriol. 174:22082214.
35. Kravanja, M.,, R. Engelmann,, V. Dossonnet,, M. Bluggel,, H. E. Meyer,, R. Frank,, A. Galinier,, J. Deutscher,, N. Schnell,, and W. Hengstenberg. 1999. The hprK gene of Enterococcus faecalis encodes a novel bifunctional enzyme: the HPr kinase/phosphatase. Mol. Microbiol. 31:5966.
36. Kuroda, M.,, T. Ohta,, I. Uchiyama,, T. Baba,, H. Yuzawa,, I. Kobayashi,, L. Cui,, A. Oguchi,, K. Aoki,, Y. Nagai,, J. Lian,, T. Ito,, M. Kanamori,, H. Matsumaru,, A. Maruyama,, H. Murakami,, A. Hosoyama,, Y. Mizutani-Ui,, N. K. Takahashi,, T. Sawano,, R. Inoue,, C. Kaito,, K. Sekimizu,, H. Hirakawa,, S. Kuhara,, S. Goto,, J. Yabuzaki,, M. Kanehisa,, A. Yamashita,, K. Oshima,, K. Furuya,, C. Yoshino,, T. Shiba,, M. Hattori,, N. Ogasawara,, H. Hayashi,, and K. Hiramatsu. 2001. Whole genome sequencing of methicillin-resistant Staphylococcus aureus. Lancet 357:12251140.
37. Maxwell, E. S.,, K. Kurahashi,, and H. M. Kalckar. 1962. Enzymes of the Leloir pathway. Methods Enzymol. 5:174189.
38. Mijakovic, I.,, S. Poncet,, A. Galinier,, V. Monedero,, S. Fieulaine,, J. Janin,, S. Nessler,, J. A. Marquez,, K. Scheffzek,, S. Hasenbein,, W. Hengstenberg,, and J. Deutscher. 2002. Pyrophosphate-producing protein dephosphorylation by HPr kinase/phosphorylase: a relic of early life? Proc. Natl. Acad. Sci. USA 99:1344213447.
39. Novick, R. P.,, S. J. Projan,, J. Kornblum,, H. F. Ross,, G. Ji,, B. Kreiswirth,, F. Vandenesch,, and S. Moghazeh. 1995. The agr P2 operon: an autocatalytic sensory transduction system in Staphylococcus aureus. Mol. Gen. Genet. 248: 446458.
40. Oskouian, B.,, and G. C. Stewart. 1990. Repression and catabolite repression of the lactose operon of Staphylococcus aureus. J. Bacteriol. 172:38043812.
41. Poolman, B.,, J. Knol,, C. van der Does,, P. J. F. Henderson,, W.-J. Liang,, G. Leblanc,, T. Pourcher,, and I. Mus-Veteau. 1996. Cation and sugar selectivity determinants in a novel family of transport proteins. Mol. Microbiol. 19:911922.
42. Postma, P. W.,, J. W. Lengeler,, and G. R. Jacobson. 1993. Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57:543594.
43. Reizer, J.,, C. Hoischen,, F. Titgemeyer,, C. Rivolta,, R. Rabus,, J. Stülke,, D. Karamata,, M. H. Saier, Jr.,, and W. Hillen. 1998. A novel protein kinase that controls carbon catabolite repression in bacteria. Mol. Microbiol. 27:11571169.
44. Reizer, J.,, S. L. Sutrina,, M. H. Saier, Jr.,, G. C. Stewart,, A. Peterkofsky,, and P. Reddy. 1989. Mechanistic and physiological consequences of HPr(ser) phosphorylation on the activities of the phosphoenolpyruvate:sugar phosphotransferase system in gram-positive bacteria: studies with site-specific mutants of HPr. EMBO J. 8:21112120.
45. Rosenstein, R.,, and F. Götz. Unpublished results.
46. Rosey, E. L.,, B. Oskouian,, and G. C. Stewart. 1991. Lactose metabolism by Staphylococcus aureus: characterization of lacABCD, the structural genes of the tagatose 6-phosphate pathway. J. Bacteriol. 173:59925998.
47. Saier, M. H., Jr.,, S. Chauvaux,, G. M. Cook,, J. Deutscher,, I. T. Paulsen,, J. Reizer,, and J.-J. Ye. 1996. Catabolite repression and inducer control in Gram-positive bacteria. Microbiology 142:217230.
48. Saier, M. H., Jr.,, S. Chauvaux,, J. Deutscher,, J. Reizer,, and J.-J. Ye. 1995. Protein phosphorylation and regulation of carbon metabolism in gram-negative versus gram-positive bacteria. Trends Biochem. Sci. 20:267271.
49. Schleifer, K. H.,, and U. Fischer. 1982. Description of a new species of the genus Staphylococcus: Staphylococcus carnosus. Int. J. Syst. Bacteriol. 32:153156.
50. Sizemore, C.,, E. Buchner,, T. Rygus,, C. Witke,, F. Götz,, and W. Hillen. 1991. Organization, promoter analysis and transcriptional regulation of the Staphylococcus xylosus xylose utilization operon. Mol. Gen. Genet. 227:377384.
51. Sizemore, C.,, B. Wieland,, F. Götz,, and W. Hillen. 1992. Regulation of Staphylococcus xylosus xylose utilization genes at the molecular level. J. Bacteriol. 174:30423048.
52. Stülke, J.,, M. Arnaud,, G. Rapoport,, and I. Martin-Verstraete. 1998. PRD—a protein domain involved in PTS-dependent induction and carbon catabolite repression of catabolic operons in bacteria. Mol. Microbiol. 28:865874.
53. Stülke, J.,, I. Martin-Verstraete,, M. Zagorec,, M. Rose,, A. Klier,, and G. Rapoport. 1997. Induction of the Bacillus subtilis ptsGHI operon by glucose is controlled by a novel antiterminator, GlcT. Mol. Microbiol. 25:6578.
54. Valentin-Hansen, P.,, P. Hojrup,, and S. Short. 1985. The primary structure of the DeoR repressor from Escherichia coli K-12. Nucleic Acids Res. 13:59275936.
55. Wagner, E.,, F. Götz,, and R. Brückner. 1993. Cloning and characterization of the scrA gene encoding the sucrose-specific enzyme II of the phosphotransferase system from Staphylococcus xylosus. Mol. Gen. Genet. 241:3341.
56. Wagner, E.,, S. Marcandier,, O. Egeter,, J. Deutscher,, F. Götz,, and R. Brückner. 1995. Glucose kinase-dependent catabolite repression in Staphylococcus xylosus. J. Bacteriol. 177:61446152.
57. Weickert, M. J.,, and S. Adhya. 1992. A family of bacterial regulators homologous to Gal and Lac repressors. J. Biol. Chem. 267:1586915874.
58. Zhang, Y. Q.,, S. X. Ren,, H. L. Li,, Y. X. Wang,, G. Fu,, J. Yang,, Z. Q. Qin,, Y. G. Miao,, W. Y. Wang,, R. S. Chen,, Y. Shen,, Z. Chen,, Z. H. Yuan,, G. P. Zhao,, D. Qu,, A. Danchin,, and Y. M. Wen. 2003. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol. Microbiol. 49:15771593.

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