Bifidobacterium longum requires a fructokinase (Frk; ATP:D-fructose 6-phosphotransferase, EC 2.7.1.4) for fructose catabolism

Journal of Bacteriology

Volumn 186, Issue 19, 2004, Pages 6515-6525

  Caescu, Cristina I ^a,b   Vidal, Olivier ^a   Krzewinski, Frédéric ^a   Artenie, Vlad ^b   Bouquelet, Stéphane ^a  

^a UNIVERSITÉ DES SCIENCES ET TECHNOLOGIES DE LILLE   (France)

^b ALEXANDRU IOAN CUZA UNIVERSITY OF IASI   (Romania)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; COBALT; DEXTRO FRUCTOSE 6 PHOSPHOTRANSFERASE; FRUCTOKINASE; FRUCTOSE; GLUCOSE; HISTIDINE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

AFFINITY CHROMATOGRAPHY; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BIFIDOBACTERIUM LONGUM; CARBOHYDRATE METABOLISM; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENZYME INDUCTION; ENZYME INHIBITION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ESCHERICHIA COLI; GENE EXPRESSION; GENE VECTOR; GENETIC CODE; GRAM POSITIVE BACTERIUM; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PRIORITY JOURNAL; TEMPERATURE;

ACTINOBACTERIA (CLASS); BACTERIA (MICROORGANISMS); BIFIDOBACTERIUM; BIFIDOBACTERIUM LONGUM; ESCHERICHIA COLI; POSIBACTERIA; UNCULTURED ACTINOMYCETE;

EID: 4544368552     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.186.19.6515-6525.2004     Document Type: Article

References (66)

1. Altschul, S. F., T. L. Madden, A. A. Schäffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Angell, S., E. Schwarz, and M. J. Bibb. 1992. The glucose kinase gene of Streptomyces coelicolor A3(2): its nucleotide sequence, transcriptional analysis and role in glucose repression. Mol. Microbiol. 6:2833-2844.
3. Aulkemeyer, P., R. Ebner, G. Heilenmann, K. Jahreis, K. Schmid, S. Wrieden, and J. W. Lengeler. 1991. Molecular analysis of two fructokinases involved in sucrose metabolism of enteric bacteria. Mol. Microbiol. 5:2913-2922.
4. Berghauser, J. 1975. A reactive arginine in adenylate kinase. Biochim. Biophys. Acta 397:370-376.
5. Bockmann, J., H. Heuel, and J. W. Lengeler. 1992. Characterization of a chromosomally encoded, non-PTS metabolic pathway for sucrose utilization in Escherichia coli EC3132. Mol. Gen. Genet. 235:22-32.
6. Bogs, J., and K. Geider. 2000. Molecular analysis of sucrose metabolism of Erwinia amylovora and influence on bacterial virulence. J. Bacteriol. 182:5351-5358.
7. Bornet, F. R., F. Brouns, Y. Tashiro, and V. Duvillier. 2002. Nutritional aspects of short-chain fructooligosaccharides: natural occurrence, chemistry, physiology and health implications. Dig. Liver Dis. 34:S111-S120.
8. Bradford, M. M. 1976. A rapid and sensitive method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
9. Brann, A., M. Tcherpakov, I. M. Williams, A. H. Futerman, and M. Fainzilber. 2002. Nerve growth factor-induced p75-mediated death of cultured hippocampal neurons is age-dependent and transduced through ceramide generated by neutral sphingomyelinase. J. Biol. Chem. 277:9812-9818.
10. Bruckner, IL, and F. Titgemeyer. 2002. Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol. Lett. 209:141-148.
11. Butler, M. J., J. Deutscher, P. W. Postma, T. J. Wilson, A. Galinier, and M. J. Bibb. 1999. Analysis of a ptsH homologue from Streptomyces coelicolor A3(2). FEMS Microbiol. Lett. 177:279-288.
12. Desjardin, L. E., L. G. Hayes, C. D. Sohaskey, L. G. Wayne, and K. D. Eisenach. 2001. Microacrophilic induction of the alpha-crystallin chaperone protein homologue (hspX) mRNA of Mycobacterium tuberculosis. J. Bacteriol. 183:5311-5316.
13. Deutscher, J., E. Kuster, U. Bergstedt, V. Charrier, and W. Hillen. 1995. Protein kinase-dependent HPr/CcpA interaction links glycolytic activity to carbon catabolite repression in gram-positive bacteria. Mol. Microbiol. 15:1049-1053.
14. de Vries, W., S. J. Gerbrandy, and A. H. Stouthamer. 1967. Carbohydrate metabolism in Bifidobacterium bifidum. Biochim. Biophys. Acta 136:415-425.
15. Ehrmann, M. A., M. Korakii, and R. F. Vogel. 2003. Identification of the gene for beta-fructofuranosidase of Bifidobacterium lactis DSM10140 (T) and characterization of the enzyme expressed in Escherichia coli. Curr. Microbiol. 46:391-397.
16. Feldheim, D. A., A. M. Chin, C. T. Nierva, B. U. Feucht, Y. W. Cao, Y. F. Xu, S. L. Sutrina, and M. H. Saier, Jr. 1990. Physiological consequences of the complete loss of phosphoryl-transfer proteins HPr and FPr of the phosphoenolpyruvate:sugar phosphotransferase system and analysis of fructose (fru) operon expression in Salmonella typhimurium. J. Bacteriol. 172:5459-5469.
17. Fennington, G. J., Jr., and T. A. Hughes. 1996. The fructokinase from Rhizobium leguminosarum biovar trifolii belongs to group I fructokinase enzymes and is encoded separately from other carbohydrate metabolism enzymes. Microbiology 142:321-330.
18. Fujita, Y., Y. Miwa, A. Galinier, and J. Deutscher. 1995. Specific recognition of the Bacillus subtilis gnt cis-acting catabolite-responsive element by a protein complex formed by CcpA and seryl-phosphorylated HPr. Mol. Microbiol. 17:953-960.
19. Henkin, T. M., F. J. Grundy, W. L. Nicholson, and G. H. Chambliss. 1991. Catabolite repression of alpha-amylase gene expression in Bacillus subtilis involves a trans-acting gene product homologous to the Escherichia coli lacI and galR repressors. Mol. Microbiol. 5:575-584.
20. Hurtado, C. A. R., and R. A. Rachubinski. 2002. Isolation and characterization of YlBEMI a gene required for cell polarization and differentiation in the dimorphic yeast Yarrowia lipolytica. Eukaryot. Cell 1:526-537.
21. Huynh, P. L., I. Jankovic, N. F. Schnell, and IL Bruckner. 2000. Characterization of an HPr kinase mutant of Staphylococcus xylosus. J. Bacteriol. 182:1895-1902.
22. Imamura, L., K. Hisamitsu, and K. Kobashi. 1994. Purification and characterization of beta-fructofuranosidase from Bifidobacterium infantis. Biol. Pharm. Bull. 17:596-602.
23. Jones, B. E., V. Dossonnet, E. Kuster, J. Deutscher, and R. E. Klevit. 1997. Binding of the catabolite repressor protein CcpA to its DNA target is regulated by phosphorylation of its corepressor HPr. J. Biol. Chem. 272:26530-26535.
24. Kaplan, H., and R. W. Hutkins. 2000. Fermentation of fructooligosaccharides by lactic acid bacteria and bifidobacteria. Appl. Environ. Microbiol. 66:2682-2684.
25. Kriebardis, T., D. Meng, and S. Aktipis. 1987. Inhibition of the RNA polymerase-catalyzed synthesis of RNA by daunomycin. Effect of the inhibitor on the late steps of RNA chain initiation. J. Biol. Chem. 262:12632-12640.
26. Krzewinski, F., C. Brassart, F. Gavini, and S. Bouquelet. 1997. Glucose and galactose transport in Bifidobacterium bifidum DSM 20082. Curr. Microbiol. 35:175-179.
27. Kwakman, J. H. J. M., and P. W. Postma. 1994. Glucose kinase has a regulatory role in carbon catabolite repression in Streptomyces coelicolor. J. Bacteriol. 176:2694-2698.
28. Luesink, E. J., J. D. Marugg, O. P. Kuipers, and W. M. de Vos. 1999. Characterization of the divergent sacBK and sacAR operons, involved in sucrose utilization by Lactococcus lactis. J. Bacteriol. 181:1924-1926.
29. Margolles, A., and C. G. de los Reyes-Gavilan. 2003. Purification and functional characterization of a novel alpha-L-arabinofuranosidase from Bifidobacterium longum B667. Appl. Environ. Microbiol. 69:5096-5103.
30. Marx, S. P., S. Winkler, and W. Hartmeier. 2000. Metabolization of beta-(2,6)-linked fructose-oligosaccharides by different bifidobacteria. FEMS Microbiol. Lett. 182:163-169.
31. Matsuki, T., K. Watanabe, R. Tanaka, M. Fukuda, and H. Oyaizu. 1999. Distribution of bifidobacterial species in human intestinal microflora examined with 16S rRNA-gene-targeted species-specific primers. Appl. Environ. Microbiol. 65:4506-4512.
32. Mitchell, W. J., J. Reizer, C. Herring, C. Hoischen, and M. H. Saier, Jr. 1993. Identification of a phosphoenolpyruvate:fructose phosphotransferase system (fructose-1-phosphate forming) in Listeria monocytogenes. J. Bacteriol. 175:2758-2761.
33. Moller, P. L., F. Jorgensen, O. C. Hansen, S. M. Madsen, and P. Stougaard. 2001. Intra- and extracellular beta-galactosidases from Bifidobacterium bifidum and B. infantis: molecular cloning, heterologous expression, and comparative characterization. Appl. Environ. Microbiol. 67:2276-2283.
34. Mondero, V., M. J. Gosalbes, and J. Perez-Martinez. 1997. Catabolite repression in Lactobacillus casei ATCC 393 is mediated by CcpA. J. Bacteriol. 179:6657-6667.
35. Nothaft, H., S. Parche, A. Kamionka, and F. Titgemeyer. 2003. In vivo analysis of HPr reveals a fructose-specific phosphotransferase system that confers high-affinity uptake in Streptomyces coelicolor. J. Bacteriol. 185:929-937.
36. Perrin, S., M. Warchol, J. P. Grill, and F. Schneider. 2001. Fermentations of fructo-oligosaccharides and their components by Bifidobacterium infantis ATCC 15697 on batch culture in semi-synthetic medium. J. Appl. Microbiol. 90:859-865.
37. Perrin, S., C. Fougnies, J. P. Grill, H. Jacobs, and F. Schneider. 2002. Fermentation of chicory fructo-oligosaccharides in mixtures of different degrees of polymerization by three strains of bifidobacteria. Can. J. Microbiol. 48:759-763.
38. Reid, S. J., M. S. Rafudeen, and N. G. Leat. 1999. The genes controlling sucrose utilization in Clostridium beijerinckii NCIMB 8052 constitute an operon. Microbiology 145:1461-1472.
39. Sabater, B., J. Sebastian, and C. Asensio. 1972. Identification and properties of an inducible and highly specific fructokinase from Streptomyces violaceoruber. Biochim. Biophys. Acta 284:414-420.
40. Sabater, B., and G. Delafuente. 1975. Kinetic properties and related changes of molecular weight in a fructokinase from Streptomyces violaceoruber. Biochim. Biophys. Acta 377:258-270.
41. Salyers, A. A., J. K. Palmer, and T. D. Wilkins. 1978. Degradation of polysaccharides by intestinal bacterial enzymes. Am. J. Clin. Nutr. 31:S128-S130.
42. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
43. Scardovi, V. 1986. Genus Bifidobacterium, p. 1418-1434. In P. H. A. Sneath, N. S. Mair, M. E. Sharpe, and J. G. Holt (ed.), Bergey's manual of systematic bacteriology, vol. 2. Williams & Wilkins, Baltimore, Md.
44. Schell, M. A., M. Karmirantzou, B. Snel, D. Vilanova, B. Berger, G. Pessi, M. C. Zwahlen, F. Desiere, P. Bork, M. Delley, R. D. Pridmore, and F. Arigoni. 2002. The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc. Natl. Acad. Sci. USA 99:14422-14427.
45. Sebastian, J., and C. Asensio. 1972. Purification and properties of the mannokinase from Escherichia coli. Arch. Biochem. Biophys. 151:227-233.
46. Skerman, V. B. D., V. McGowan, and P. H. A. Sneath. 1980. Approved lists of bacterial names. Int. J. Syst. Bacteriol. 30:225-420.
47. Spath, C., A. Kraus, and W. Hillen. 1997. Contribution of glucose kinase to glucose repression of xylose utilization in Bacillus megaterium. J. Bacteriol. 179:7603-7605.
48. Sprogoe, D., L. A. Van Den Broek, O. Mirza, J. S. Kastrup, A. G. Voragen, M. Gajhede, and L. K. Skov. 2004. Crystal structure of sucrose phosphorylase from Bifidobacterium adolescentis. Biochemistry 43:1156-1162.
49. Sproul, A. A., L. T. Lambourne, D. J. Jean-Jacques, and H. L. Kornberg. 2001. Genetic control of manno(fructo)kinase activity in Escherichia coli. Proc. Natl. Acad. Sci. USA 98:15257-15259.
50. Studier, F. W., A. H. Rosenberg, and J. J. Dunn. 1990. Use of T7 RNA polymerase to direct the expression of cloned genes. Methods Enzymol. 185:60-89.
51. Tanaka, H., H. Hashiba, J. Kok, and I. Mierau. 2000. Bile salt hydrolase of Bifidobacterium longum: biochemical and genetic characterization. Appl. Environ. Microbiol. 66:2502-2512.
52. Thompson, J., and B. M. Chassy. 1981. Uptake and metabolism of sucrose by Streptococcus lactis. J. Bacteriol. 147:543-551.
53. Thompson, J., D. L. Sackett, and J. A. Donkersloot. 1991. Purification and properties of fructokinase I from Lactococcus lactis. Localization of scrK on the sucrose-nisin transposon Tn5306. J. Biol. Chem. 266:22626-22633.
54. Thompson, J., N. Y. Nguyen, and S. A. Robrish. 1992. Sucrose fermentation by Fusobacterium mortiferum ATCC 25557: transport, catabolism, and products. J. Bacteriol. 174:3227-3235.
55. Titgemeyer, F., J. Reizer, A. Reizer, and M. H. Jr., Saier. 1994. Evolutionary relationships between sugar kinases and transcriptional repressors in bacteria. Microbiology 140:2349-2354.
56. Trindade, M. I., V. R. Abratt, and S. J. Reid. 2003. Induction of sucrose utilization genes from Bifidobacterium lactis by sucrose and raffinose. Appl. Environ. Microbiol. 69:24-32.
57. Van Den Bogaard, P. T. C., M. Kleerebezem, O. Kuipers, and W. M. de Vos. 2000. Control of lactose transport, β-galactosidase activity, and glycolysis by CcpA in Streptococcus thermophilus: evidence for carbon catabolite repression by a non-phosphoenolpyruvate-dependent phosphotransferase system sugar. J. Bacteriol. 182:5982-5989.
58. Van Den Broek, L. A., E. L. Van Boxtel, R. P. Kievit, R. Verhoef, G. Beldman, and A. G. Voragen. 2004. Physico-chemical and transglucosylation properties of recombinant sucrose phosphorylase from Bifidobacterium adolescentis DSM20083. Appl. Microbiol. Biotechnol. 61:55-60.
59. Veerkamp, J. H. 1969. Catabolism of glucose and derivatives of 2-deoxy-2-amino-glucose in Bifidobacterium bifidum var. pennsylvanicus. Arch. Biochem. Biophys. 129:257-263.
60. Wade, H. E., and D. M. Morgan. 1953. Detection of phosphate esters on paper chromatograms. Nature 171:529-530.
61. Wagner, E., S. Marcandier, O. Egeter, J. Deutscher, F. Götz, and R. Brückner. 1995. Glucose kinase-dependent catabolite repression in Staphylococcus xylosus. J. Bacteriol. 177:6144-6152.
62. Wagner, E., E. Küster-Schöck, and W. Hillen. 2000. Sugar uptake and carbon catabolite repression in Bacillus megaterium strains with inactivated ptsHI. J. Mol. Microbiol. Biotechnol. 2:587-592.
63. Warchol, M., S. Perrin, J. P. Grill, and F. Schneider. 2002. Characterization of a purified beta-fructofuranosidase from Bifidobacterium infantis ATCC 15697. Lett. Appl. Microbiol. 35:462-467.
64. Weisser, P., R. Kramer, H. Sahm, and G. A. Sprenger. 1995. Functional expression of the glucose transporter of Zymomonas mobilis leads to restoration of glucose and fructose uptake in Escherichia coli mutants. J. Bacteriol. 177:3351-3354.
65. Weisser, P., R. Kramer, and G. A. Sprenger. 1996. Expression of the Escherichia coli pmi gene, encoding phosphomannose-isomerase in Zymomonas mobilis, leads to utilization of mannose as a novel growth substrate, which can be used as a selective marker. Appl. Environ. Microbiol. 62:4155-4161.
66. Zembrzuski, B., P. Chilco, X. L. Liu, J. Liu, T. Conway, and R. Scopes. 1992. Cloning, sequencing, and expression of the Zymomonas mobilis fructokinase gene and structural comparison of the enzyme with other hexose kinases. J. Bacteriol. 174:3455-3460.