Applied Microbiology and Biotechnology

, Volume 67, Issue 3, pp 312–321 | Cite as

Sucrose utilisation in bacteria: genetic organisation and regulation

  • Sharon J. ReidEmail author
  • Valerie R. Abratt


Sucrose is the most abundant disaccharide in the environment because of its origin in higher plant tissues, and many Eubacteria possess catalytic enzymes, such as the sucrose-6-phosphate hydrolases and sucrose phosphorylases, that enable them to metabolise this carbohydrate in a regulated manner. This review describes the range of gene architecture, uptake systems, catabolic activity and regulation of the sucrose-utilisation regulons that have been reported in the Eubacteria to date. Evidence is presented that, although there are many common features to these gene clusters and high conservation of the proteins involved, there has been a certain degree of gene shuffling. Phylogenetic analyses of these proteins supports the hypothesis that these clusters have been acquired through horizontal gene transfer via mobile elements and transposons, and this may have enabled the recipient bacteria to colonise sucrose-rich environmental niches.


Lactic Acid Bacterium Hydrolase Catabolite Repression Leuconostoc Mesenteroides Clostridium Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Supplementary material

Table S1 Accession Numbers of DNA sequence and proteins used in phylogenetic analysis

253_2004_1885_ESM_supp.pdf (16 kb)
(PDF 17 KB)


  1. Barrangou R, Altermann E, Hutkins R, Cano R, Klaenhammer TR (2003) Functional and comparative genomic analyses of an operon involved in fructooligosaccharide utilization by Lactobacillus acidophilus. Proc Natl Acad Sci USA 100:8957–8962CrossRefGoogle Scholar
  2. Blatch GL, Woods DR (1991) Nucleotide sequence and analysis of the Vibrio alginolyticus scr repressor-encoding gene (scrR). Gene 101:45–50CrossRefGoogle Scholar
  3. Blatch GL, Woods DR (1993) Molecular characterization of a fructanase produced by Bacteroides fragilis BF-1. J Bacteriol 175:3058–3066Google Scholar
  4. Bogs J, Geider K (2000) Molecular analysis of sucrose metabolism of Erwinia amylovora and influence on bacterial virulence. J Bacteriol 182:5351–5358CrossRefGoogle Scholar
  5. Broek LAM van den, van Boxtel EL, Kievit RP, Verhoef R, Beldman G, Voragen AGJ (2004) Physico-chemical and transglucosylation properties of recombinant sucrose phosphorylase from Bifidobacterium adolescentis DSM20083. Appl Microbiol Biotechnol 65:219–227CrossRefGoogle Scholar
  6. Brückner R, Titgemeyer F (2002) Carbon catabolite repression in bacteria: choice of the carbon source and autoregulatory limitation of sugar utilization. FEMS Microbiol Lett 209:141–148CrossRefGoogle Scholar
  7. Brückner R, Wagner E, Gotz F (1993) Characterization of a sucrase gene from Staphylococcus xylosus. J Bacteriol 175:851–857Google Scholar
  8. Busby S, Ebright RH (1999) Transcription activation by catabolite activator protein (CAP). J Mol Biol 293:199–213CrossRefGoogle Scholar
  9. Davison SP, Santangelo JD, Reid SJ, Woods DR (1995) A Clostridium acetobutylicum regulator gene (regA) affecting amylase production in Bacillus subtilis. Microbiol 141:989–996Google Scholar
  10. Deutscher J, Galinier A, Martin-Verstraete I (2002) Carbohydrate uptake and metabolism. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and its closest relatives: from genes to cells. ASM, Washington, pp 129–150Google Scholar
  11. Dols M, Chraibi W, Remaud-Simeon M, Lindley ND, Monsan PF (1997) Growth and energetics of Leuconostoc mesenteroides NRRL B-1299 during metabolism of various sugars and their consequences for dextransucrase production. Appl Environ Microbiol 21:59–65Google Scholar
  12. Doolittle WF (1999) Phylogenetic classification and the universal tree. Science 284:2124–2128CrossRefGoogle Scholar
  13. Egeter O, Brückner R (1996) Catabolite repression mediated by the catabolite control protein CcpA in Staphylococcus xylosus. Mol Microbiol 21:739–749CrossRefGoogle Scholar
  14. Fitzgerald JR, Sturdevant DE, Mackie SM, Gill SR, Musser JM (2001) Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc Natl Acad Sci USA 98:8821–8826CrossRefGoogle Scholar
  15. Fouet A, Klier AF, Rapoport G (1986) Nucleotide sequence of the sucrase gene of Bacillus subtilis. Gene 45:221–225CrossRefGoogle Scholar
  16. Fournier P, de Ruffray P, Otten L (1994) Natural instability of Agrobacterium vitis Ti plasmid due to unusual duplication of a 2.3-kb DNA fragment. Mol Plant–Microb Interact 7:164–172Google Scholar
  17. Gering M, Brückner R (1996) Transcriptional regulation of the sucrase gene of Staphylococcus xylosus by the repressor ScrR. J Bacteriol 178:462–469Google Scholar
  18. Henkin TM, Grundy FJ, Nicholson WL, Chambliss GH (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 5:575–584Google Scholar
  19. Henrissat B, Bairoch A (1996) Updating the sequence-based classification of glycosyl hydrolases. Biochem J 316:695–696PubMedGoogle Scholar
  20. Hiratsuka K, Wang B, Sato Y, Kuramitsu H (1998) Regulation of sucrose-6-P hydrolase activity in Streptococcus mutans: characterization of the scrR gene. Infect Immun 66:3736–3743Google Scholar
  21. Hochhut B, Jahreis K, Lengeler JW, Schmid K (1997) CTnscr94, a conjugative transposon found in enterobacteria. J Bacteriol 179:2097–2102Google Scholar
  22. Hueck CJ, Hillen W (1995) Catabolite repression is Bacillus subtilis: a global regulatory mechanism for the Gram-positive bacteria? Mol Microbiol 15:395–401Google Scholar
  23. Jahreis K, Bentler L, Bockmann J, Hans S, Meyer A, Siepelmeyer J, Lengeler JW (2002) Adaptation of sucrose metabolism in the Escherichia coli wild-type strain EC3132. J Bacteriol 184:5307–5316CrossRefGoogle Scholar
  24. Kawasaki H, Nakamura N, Ohmori M, Sakai T (1996) Cloning and expression in E. coli of sucrose phosphorylase gene from Leuconostoc mesenteroides no. 165. Biosci Biotechnol Biochem 60:322–324Google Scholar
  25. Kim M, Kwon T, Lee HJ, Kim KH, Chung DK, Ji GE, Byeon ES, Lee JH (2003) Cloning and expression of sucrose phosphorylase gene from Bifidobacterium longum in E. coli and characterization of the recombinant enzyme. Biotechnol Lett 25:1211–1217CrossRefGoogle Scholar
  26. Kitaoka M, Hayashi K (2002) Carbohydrate-processing phosphorolytic enzymes. Trends Glycosci Glycotechnol 14:35–50Google Scholar
  27. Koga T, Nakamura K, Shirokane Y, Mizusawa K, Kitao S, Kikuchi M (1991) Purification and some properties of sucrose phosphorylase from Leuconostoc mesenteroides. Agric Biol Chem 55:1805–1810Google Scholar
  28. Laere KMJ van, Hartemink R, Bosveld M, Schols HA, Voragen AGJ (2000) Fermentation of plant cell wall derived polysaccharides and their corresponding oligosaccharides by intestinal bacteria. J Agric Food Sci 48:1644–1652CrossRefGoogle Scholar
  29. Lengeler JW, Jahreis K, Wehmeier UF (1994) Enzymes II of the phosphoenolpyruvate-dependent phosphotransferase systems: their structure and function in carbohydrate transport. Biochim Biophys Acta 1188:1–28Google Scholar
  30. Liebl W, Brem D, Gotschlich A (1998) Analysis of the gene for beta-fructosidase (invertase, inulinase) of the hyperthermophilic bacterium Thermotoga maritima, and characterisation of the enzyme expressed in Escherichia coli. Appl Microbiol Biotechnol 50:55–64CrossRefGoogle Scholar
  31. Luesink EJ, Marugg JD, Kuipers OP, de Vos WM (1999) Characterisation of the divergent sacBK and sacAR operons, involved in sucrose utilisation in Lactococcus lactis. J Bacteriol 181:1924–1926Google Scholar
  32. Moreno MS, Schneider BL, Maile RR, Weyler W, Saier MH Jr (2001) Catabolite repression mediated by the CcpA protein in Bacillus subtilis: novel modes of regulation revealed by whole-genome analyses. Mol Microbiol 39:1366–1381Google Scholar
  33. Naumoff DG, Livshits VA (2001) Molecular structure of the Lactobacillus plantarum sucrose utilization locus: comparison with Pediococcus pentosaceus. Mol Biol 35:15–22CrossRefGoogle Scholar
  34. Nesbo CL, Nelson KE, Doolittle WF (2002) Suppressive subtractive hybridization detects extensive genomic diversity in Thermotoga maritima. J Bacteriol 184:4475–4488CrossRefGoogle Scholar
  35. Nolling J, Breton G, Omelchenko MV, Makarova KS, Zeng Q, Gibson R, Lee HM, Dubois J, Qiu D, Hitti J, Wolf YI, Tatusov RL, Sabathe F, Doucette-Stamm L, Soucaille P, Daly MJ, Bennett GN, Koonin EV, Smith DR (2001) Genome sequence and comparative analysis of the solvent-producing bacterium Clostridium acetobutylicum. J Bacteriol 183:4823–4838CrossRefPubMedGoogle Scholar
  36. Ochman H, Lawrence JG, Groisman EA (2000) Lateral gene transfer and the nature of bacterial innovation. Nature 405:299–304CrossRefPubMedGoogle Scholar
  37. Parche S, Burkovski A, Sprenger GA, Weil B, Kramer R, Titgemeyer, F (2001) Corynebacterium glutamicum: a dissection of the PTS. J Mol Microbiol Biotechnol 3:423–428Google Scholar
  38. Pareira Y, Petit-Glatron M, Chambert R (2001) yveB, encoding endolevanase LevB, is part of the sacByveByveA levansucrase tricistronic operon in B. subtilis. Microbiol 147:3413–3419Google Scholar
  39. Paulsen IT (1996) Carbon metabolism and its regulation in Streptomyces and other high GC Gram-positive bacteria. Res Microbiol 147:535–541CrossRefGoogle Scholar
  40. Rauch PJG, de Vos WM (1992) Transcriptional regulation of the Tn5276-located Lactococcus lactis sucrose operon and characterisation of the sacA gene encoding sucrose-6-phosphate hydrolase. Gene 121:55–61CrossRefGoogle Scholar
  41. Rauch PJG, Beerthuyzen MM, de Vos WM (1994) Distribution and evolution of nisin–sucrose elements in Lactococcus lactis. Appl Environ Microbiol 60:1798–1804Google Scholar
  42. Reid SJ (2004) Genetic organisation and regulation of hexose and pentose utilisation in the Clostridia. In: Duerre P (ed) The Clostridia. CRC, Boca Raton (in press)Google Scholar
  43. Reid SJ, Rafudeen MS, Leat NG (1999) The genes controlling sucrose utilization in Clostridium beijerinckii NCIMB 8052 constitute an operon. Microbiol 145:1461–1471Google Scholar
  44. Reizer J, Romano AH, Deutscher J (1993) The role of phosphorylation of HPr, a phosphocarrier protein of the phosphotransferase system, in the regulation of carbon metabolism in Gram-positive bacteria. J Cell Biol Chem 51:19–24Google Scholar
  45. Russell RR, Mukasa H, Shimamura A, Ferretti JJ (1988) Streptococcus mutans gtfA gene specifies sucrose phosphorylase. Infect Immun 56:2763–2765Google Scholar
  46. Russell RR, Aduse-Opoku J, Sutcliffe IC, Tao L, Ferretti JJ (1992) A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. J Biol Chem 267:4631–4637Google Scholar
  47. Rutberg B (1997) Antitermination of transcription of catabolic operons. Mol Microbiol 23:413–421CrossRefGoogle Scholar
  48. Saier MH (1998) Molecular phylogeny as a basis for the classification of transport proteins from bacteria, archaea and eukarya. Adv Microbiol Physiol 40:81–136Google Scholar
  49. Saier MH, Fagan MJ, Hoischen C, Reizer J (1993) Transport mechanisms. In: Sonenshein AL, Hoch JA, Losick R (eds) Bacillus subtilis and other Gram-positive bacteria: biochemistry, physiology and molecular genetics. ASM, Washington, pp 133–156Google Scholar
  50. Saier MH, Chauvaux S, Deutscher J, Reizer J, Ye J-J (1995) Protein phosphorylation and regulation of carbon metabolism in Gram-negative versus Gram-positive bacteria. Trends Biochem Sci 20:267–271CrossRefGoogle Scholar
  51. Schell MA, Karmirantzou M, Snel B, Vilanova D, Berger B, Pessi G, Zwahlen M, Desiere F, Bork P, Delley M, Pridmore RD, Arigoni F (2002) The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proc Natl Acad Sci USA 99:14422–14427Google Scholar
  52. Schmid K, Ebner R, Altenbuchner J, Schmitt R, Lengeler JW (1988) Plasmid-mediated sucrose metabolism in E. coli K12: mapping of the scr genes of pUR400. Mol Microbiol 2:1–8Google Scholar
  53. Shimizu T, Ohtani K, Hirakawa H, Ohshima K, Yamashita A, Shiba T, Ogasawara N, Hattori M, Kuhara S, Hayashi H (2002) Complete genome sequence of Clostridium perfringens, an anaerobic flesh-eater. Proc Natl Acad Sci USA 99:996–1001CrossRefPubMedGoogle Scholar
  54. Song EK, Kim H, Sung HK, Cha J (2002) Cloning and characterization of a levanbiohydrolase from Microbacterium laevaniformans ATCC 15953. Gene 291:45–55CrossRefGoogle Scholar
  55. Sprogoe D, van den Broek LA, Mirza O, Kastrup JS, Voragen AG, Gajhede M, Skov LK (2004) Crystal structure of sucrose phosphorylase from Bifidobacterium adolescentis. Biochemistry 43:1156–1162CrossRefGoogle Scholar
  56. Steinmetz M (1993) Carbohydrate catabolism: pathways, enzymes, genetic regulation, and evolution. In: Sonenshein AL (ed) Bacillus subtilis and other Gram-positive bacteria: biochemistry, physiology and molecular genetics. ASM, Washington, pp 157–170Google Scholar
  57. Sutrina SI, Reddy P, Saier MH, Reizer J (1990) The glucose permease of Bacillus subtilis is a single polypeptide chain that functions to energize the sucrose permease. J Biol Chem 265:18581–18589Google Scholar
  58. Tangney M, Mitchell WJ (2000) Analysis of a catabolic operon for sucrose transport and metabolism in Clostridium acetobutylicum ATCC 824. J Mol Microbiol Biotechnol 2:71–80Google Scholar
  59. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680PubMedGoogle Scholar
  60. Titgemeyer F, Reizer J, Reizer A, Saier MH (1994) Evolutionary relationships between sugar kinases and transcriptional repressors in bacteria. Microbiology 140:2349–2354Google Scholar
  61. Titgemeyer F, Jahreis K, Ebner R, Lengeler JW (1996) Molecular analysis of the scrA and scrB genes from Klebsiella pneumoniae and plasmid pUR400, which encode the sucrose transport protein Enzyme II(Scr) of the phosphotransferase system and a sucrose-6-phosphate invertase. Mol Gen Genet 250:197–206CrossRefGoogle Scholar
  62. Tortosa P, Declerck N, Dutartre H, Lindner C, Deutscher J, Le Coq D (2001) Sites of positive and negative regulation in the Bacillus subtilis antiterminators LicT and SacY. Mol Microbiol 41:1381–1383CrossRefGoogle Scholar
  63. Trethewey RN, Fernie AR, Bachmann A, Fleicscher-Notter H, Geigenberger P, Willmitzer L (2001) Expression of a bacterial phosphorylase in potato tubers results in a glucose independent induction of glycolysis. Plant Cell Environ 24:357–365CrossRefGoogle Scholar
  64. Trindade MI, Abratt VR, Reid SJ (2003) Induction of the sucrose utilisation genes from Bifidobacterium lactis by sucrose and raffinose. Appl Environ Microbiol 69:24–32CrossRefGoogle Scholar
  65. Weickert MJ, Adhya S (1992) The family of bacterial regulators homologous to Gal and Lac repressors. J Biol Chem 267:15869–15874Google Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Department of Molecular and Cell BiologyUniversity of Cape TownCape TownSouth Africa

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