Molecular and biochemical characterization of a β-fructofuranosidase from Xanthophyllomyces dendrorhous

Applied and Environmental Microbiology

Volumn 75, Issue 4, 2009, Pages 1065-1073

  Linde, Dolores ^a   Macias, Isabel ^a   Fernández Arrojo, Lucía ^b   Plou, Francisco J ^b   Jiménez, Antonio ^a   Fernández Lobato, María ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

^b INSTITUTO DE CATÁLISIS Y PETROLEOQUÍMICA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS THALIANA; BIOCHEMICAL CHARACTERIZATIONS; CATALYTIC EFFICIENCIES; EXTRACELLULAR; FRUCTOOLIGOSACCHARIDE; GLYCOSYL; HYDROLASES; KESTOSE; N-LINKED; OPTIMUM ACTIVITIES; SACCHAROMYCES CEREVISIAE; STRUCTURAL MODELS; SUCROSE SOLUTIONS; THERMOPHILICITY; TRANSGLYCOSYLATION; XANTHOPHYLLOMYCES DENDRORHOUS;

AMINES; AMINO ACIDS; CARBOHYDRATES; ENZYMES; MODEL STRUCTURES; ORGANIC ACIDS; ORGANIC COMPOUNDS; SUGAR (SUCROSE); YEAST;

ENZYME ACTIVITY;

AMINO ACID; BIOCHEMISTRY; CARBOHYDRATE; DICOTYLEDON; ENZYME ACTIVITY; HYDROLYSIS; MOLECULAR ANALYSIS; MUTATION; PH; PHYLOGENETICS; THERMOPHILY; YEAST;

BASIDIOMYCOTA; BETA-FRUCTOFURANOSIDASE; DNA, FUNGAL; ENZYME STABILITY; FUNGAL PROTEINS; GLYCOPROTEINS; HYDROGEN-ION CONCENTRATION; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; OLIGOSACCHARIDES; PHYLOGENY; PROTEIN STRUCTURE, TERTIARY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; SUCROSE; TEMPERATURE; TRISACCHARIDES;

ARABIDOPSIS THALIANA; SACCHAROMYCES CEREVISIAE; XANTHOPHYLLOMYCES DENDRORHOUS;

EID: 59949084803     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.02061-08     Document Type: Article

References (61)

1. Alberto, F., E. Jordi, B. Henrissat, and M. Czjzek. 2006. Crystal structure of inactivated Thermotoga maritima invertase in complex with the trisaccharide substrate raffinose. Biochem. J. 395:457-462.
2. Álvaro-Benito, M., M. A. de Abreu, L. Fernández-Arrojo, F. J. Plou, J. Jiménez-Barbero, A. Ballesteros, J. Polaina, and M. Fernández-Lobato. 2007. Characterization of a β- fructofuranosidase from Schwanniomyces occidentalis with transfructosylating activity yielding the prebiotic 6-kestose. J. Biotechnol. 132:75-81.
3. Antosova, M., and M. Polakovic. 2001. Fructosyltransferases: the enzymes catalyzing production of fructooligosaccharides. Chem. Pap.-Chem. Zvesti. 55:350-358.
4. Bang, M. L., I. Villadsen, and T. Sandal. 1999. Cloning and characterization of an endo-β-1,3(4)glucanase and an aspartic protease from Phaffia rhodozyma CBS 6938. Appl. Microbiol. Biotechnol. 51:215-222.
5. Belcarz, A., G. Ginalska, J. Lobarzewski, and C. Penel. 2002. The novel non-glycosylated invertase from Candida utilis (the properties and the conditions of production and purification). Biochim. Biophys. Acta 1594:40-53.
6. Bendtsen, J. D., H. Nielsen, G. von Heijne, and S. Brunak. 2004. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340:783-795.
7. Castillo, A., and V. Cifuentes. 1994. Presence of double-stranded RNA and virus-like particles in Phaffia rhodozyma. Curr. Genet. 26:364-368.
8. Chávez, F. P., T. Pons, J. M. Delgado, and L. Rodriguez. 1998. Cloning and sequence analysis of the gene encoding invertase (INV1) from the yeast Candida utilis. Yeast 14:1223-1232.
9. Díaz, A., C. Sieiro, and T. G. Villa. 2003. Production and partial characterization of a beta-amylase by Xanthophyllomyces dendrorhous. Lett. Appl. Biotechnol. 36:203-207.
10. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
11. Farine, S., C. Versluis, P. J. Bonnici, A. Heck, C. L'Homme, A. Puigserver, and A. Biagini. 2001. Application of high performance anion exchange chromatography to study invertase-catalysed hydrolysis of sucrose and formation of intermediate fructan products. Appl. Microbiol. Biotechnol. 55:55-60.
12. Fernández Arrojo, L., D. Marín, A. Gómez de Segura, D. Linde, M. Alcalde, P. Gutiérrez Alonso, F. J. Plou, M. Fernández-Lobato, and A. Ballesteros. 2007. Transformation of maltose into prebiotic isomaltooligosaccharides by a novel alpha-glucosidase from Xanthophyllomyces dendrorhous. Process Biochem. 42:1530-1536.
13. Fujishima, M., H. Sakai, K. Ueno, N. Takahashi, S. Onodera, N. Benkeblia, and N. Shiomi. 2005. Purification and characterization of a fructosyltransferase from onion bulbs and its key role in the synthesis of fructo-oligosaccharides in vivo. New Phytol. 165:513-524.
14. Gascón, S., N. P. Neumann, and J. O. Lampen. 1968. Comparative study of the properties of the purified internal and external invertases from yeast. J. Biol. Chem. 243:1573-1577.
15. Ghazi, I., L. Fernández-Arrojo, H. Garcia-Arellano, F. J. Plou, and A. Ballesteros. 2007. Purification and kinetic characterization of a fructosyltransferase from Aspergillus aculeatus. J. Biotechnol. 128:204-211.
16. Goetz, M., and T. Roitsch. 1999. The different pH optima and substrate specificities of extracellular and vacuolar invertases from plants are determined by a single amino-acid substitution. Plant J. 20:707-711.
17. Golubev, W. I. 1995. Perfect state of Rhodomyces dendrorhous (Phaffia rhodozyma). Yeast 11:101-110.
18. Goosen, C., X. L. Yuan, J. M. van Munster, A. F. Ram, M. J. van der Maarel, and L. Dijkhuizen. 2007. Molecular and biochemical characterization of a novel intracellular invertase from Aspergillus niger with transfructosylating activity. Eukaryot. Cell 6:674-681.
19. Hayashi, S., T. Yoshiyama, N. Fujii, and S. Shinohara. 2000. Production of a novel syrup containing neofructo-oligosaccharides by the cells of Penicillium citrinum. Biotechnol. Lett. 22:1465-1469.
20. Hernalsteens, S., and F. Maugeri. 2008. Purification and characterisation of a fructosyltransferase from Rhodotorula sp. Appl. Microbiol. Biotechnol. 79:589-596.
21. Heyer, A. G., and R. Wendenburg. 2001. Gene cloning and functional characterization by heterologous expression of the fructosyltransferase of Aspergillus sydowi IAM 2544. Appl. Environ. Microbiol. 67:363-370.
22. Hidaka, H., M. Hirayama, and N. Sumi. 1988. A fructooligosaccharides-producing enzyme from Aspergillus niger ATCC 20611. Agric. Biol. Chem. 52:1181-1187.
23. Hirayama, M., N. Sumi, and H. Hidaka. 1989. Purification and properties of a fructooligosaccharide-producing beta-fructofuranosidase from Aspergillus niger ATCC-20611. Agric. Biol. Chem. 53:667-673.
24. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
25. Johnson, E. A. 2003. Phaffia rhodozyma: colorful odyssey. Int. Microbiol. 6:169-174.
26. Katapodis, P., and P. Christakopoulos. 2004. Induction and partial characterization of intracellular β-fructofuranosidase from Thermoascus aurantiacus and its application in the synthesis of 6-kestose. World J. Microbiol. Biotechnol. 20:667-672.
27. Katapodis, P., E. Kalogeris, D. Kekos, B. J. Macris, and P. Christakopoulos. 2004. Biosynthesis of fructo-oligosaccharides by Sporotrichum thermophile during submerged batch cultivation in high sucrose media. Appl. Microbiol. Biotechnol. 63:378-382.
28. Kaur, N., and A. K. Gupta. 2002. Applications of inulin and oligofructose in health and nutrition. J. Biosci. 27:703-714.
29. Kilian, S., S. Kritzinger, C. Rycroft, G. Gibson, and J. du Preez. 2002. The effects of the novel bifidogenic trisaccharide, neokestose, on the human colonia microbiota. 2002. World J. Microbiol. Biotechnol. 18:637-644.
30. Kritzinger, S. M., S. G. Kilian, M. A. Potgieter, and J. C. du Preez. 2003. The effect of production parameters on the synthesis of the prebiotic trisaccharide, neokestose, by Xanthophyllomyces dendrorhous (Phaffia rhodozyma). Enz. Microbial Technol. 32:728-737.
31. Lim, J. S., S. W. Park, J. W. Lee, et al. 2005. Immobilization of Penicillium citrinum by entrapping cells in calcium alginate for the production of neofructooligosaccharides. J. Microbiol. Biotechnol. 15:1317-1322.
32. Lim, J. S., J. H. Lee, S. W. Kang, S. W. Park, and S. W. Kim. 2007. Studies on production and physical properties of neo-FOS produced by co-immobilized Penicillium citrinum and neo-fructosyltransferase. Eur. Food Res. Technol. 225:457-462.
33. Marín, D., D. Linde, and M. Fernández-Lobato. 2006. Purification and biochemical characterization of a Xanthophyllomyces dendrorhous alpha-glucosidase. Yeast 23:117-125.
34. 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.
35. Meng, G., and K. Fütterer. 2008. Donor substrate recognition in the raffinose-bound E342A mutant of fructosyltransferase Bacillus subtilis levansucrase. BMC Struct. Biol. 8:16-27.
36. Moreno, S., Y. Sánchez, and L. Rodríguez. 1990. Purification and characterization of the invertase from Schizosaccharomyces pombe. Biochem. J. 267: 697-702.
37. Nagem, R. A. P., A. L. Rojas, A. M. Golubev, O. S. Korneeva, E. V. Eneyskaya, A. A. Kulminskaya, K. N. Neustroev, and I. Polikarpov. 2004. Crystal structure of exo-inulinase from Aspergillus awamori: the enzyme fold and structural determinants of substrate recognition. J. Mol. Biol. 344:471-480.
38. Ochman, H., A. S. Gerber, and D. L. Hatl. 1988. Genetic applications of an inverse polymerase chain reaction. Genetics 120:621-623.
39. Park, M. C., J. S. Lim, J. C. Kim, S. W. Park, and S. W. Kim. 2005. Continuous production of neo-fructooligosaccharides by immobilization of whole cells of Penicillium citrinum. Biotechnol. Lett. 27:127-130.
40. Pérez, J. A., J. Rodríguez, L. Rodríguez, and T. Ruiz. 1996. Cloning and sequence analysis of the invertase gene INV1 from the yeast Pichia anomala. Curr. Genet. 29:234-240.
41. Persike, S. D., T. M. B. Bonfirm, M. R. H. Santos, S. M. O. Ling, M. D. Chiarello, and J. D. Fontana. 2002. Invertase and urease activities in carogenogenetic yeast Xanthophyllomyces dendrorhous (formerly Phaffia rhodozyma). Bioresour. Technol. 82:79-85.
42. Plou, F. J., A. Ǵmez de Segura, and A. Ballesteros. 2007. Application of glycosidases and transglycosidases for the synthesis of oligosaccharides., p. 141-157. In J. Polaina and A. P. MacCabe (ed.), Industrial enzymes: structure, function, and applications. Springer, New York, NY.
43. Pons, T., D. G. Naumoff, C. Martínez-Fleites, and L. Hernández. 2004. Three acidic residues are at the active site of a beta-propeller architecture in glycoside hydrolase families 32, 43, 62, and 68. Proteins 54:424-432.
44. Rao, A. V. 1999. Dose-response effects of inulin and oligofructose on intestinal bifidogenesis effects. J. Nutr. 129(Suppl. 7):1442S-1445S.
45. Reddy, V. A., and F. Maley. 1990. Identification of an active-site residue in yeast invertase by affinity labelling and site-directed mutagenesis. J. Biol. Chem. 265:10817-10820.
46. Reddy, A., and F. Maley. 1996. Studies on identifying the catalytic role of Glu-204 in the active site of yeast invertase. J. Biol. Chem. 271:13953-13957.
47. Rehm, J., L. Willmitzer, and A. G. Heyer. 1998. Production of 1-kestose in transgenic yeast expressing a fructosyltransferase from Aspergillus foetidus. J. Bacteriol. 180:1305-1310.
48. Ritsema, T., L. Hernández, A. Verhaar, D. Altenbach, T. Boller, A. Wiemken, and S. Smeekens. 2006. Developing fructan-synthesizing capability in a plant invertase via mutations in the sucrose-binding box. Plant J. 48:228-237.
49. Rodríguez, J., J. A. Pérez, T. Ruiz, and L. Rodríguez. 1995. Characterization of the invertase from Pichia anomala. Biochem. J. 306:235-239.
50. Sali, A., and T. L. Blundell. 1993. Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
51. Sambrook, K. J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
52. Sangeetha, P. T., M. N. Ramesh, and S. G. Prapulla. 2005. Fructooligosaccharide production using fructosyl transferase obtained from recycling culture of Aspergillus oryzae CFR 202. Process Biochem. 40:1085-1088.
53. Ueno, K., S. Onodera, A. Kawakami, M. Yoshida, and N. Shiomi. 2005. Molecular characterization and expression of a cDNA encoding fructan: fructan 6G-fructosyltransferase from asparagus (Asparragus officinalis). New Phytol. 165:813-824.
54. Van der Westhuizen, R. J. 2008. The potential of neokestose as a prebiotic for broiler chickens. Magister's thesis. University of the Free State, Bloemfontein, South Africa.
55. Verhaest, M., W. Lammens, K. Le Roy, B. De Coninck, C. J. De Ranter, A. Van Laere, W. Van den Ende, and A. Rabijns. 2006. X-ray diffraction structure of a cell-wall invertase from Arabidopsis thaliana. Biol. Crystallogr. 62:1555-1563.
56. Verdoes, J. C., J. Wery, T. Boekhout, and A. J. Van Ooyen. 1997. Molecular characterization of the glyceraldehyde-3-phosphate dehydrogenase gene of Phaffia rhodozyma. Yeast 13:1231-1242.
57. Vernet, T., D. Dignard, and D. Y. Thomas. 1987. A family of yeast expression vectors containing the phage f1 intergenic region. Gene 52:225-233.
58. Vijn, I., and S. Smeekens. 1999. Fructan: more than a reserve carbohydrate? Plant Physiol. 120:351-359.
59. Voegele, R. T., S. Wirsel, U. Möll, M. Lechner, and K. Mendgen. 2006. Cloning and characterization of a novel invertase from the obligate biotroph Uromyces fabae and analysis of expression patterns of host and pathogen invertases in the course of infection. Mol. Plant-Microbe Interact. 19:625-634.
60. Wery, J., M. J. Dalderup, J. Ter Linde, T. Boekhout, A. J. Van Ooyen. 1996. Structural and phylogenetic analysis of the actin gene from the yeast Phaffia rhodozyma. Yeast 12:641-651.
61. Yanase, H., M. Maeda, E. Hagiwara, H. Yagi, K. Taniguchi, and K. Okamoto. 2002. Identification of functionally important amino acid residues in Zymomonas mobilis levansucrase. J. Biochem. 132:565-572.