Structural Characterization of Non-reducing Oligosaccharide Produced by Arthrobacter crystallopoietes N-08

  • Bae, Bum-Sun (Department of Food Science and Biotechnology, Kyonggi University) ;
  • Shin, Kwang-Soon (Department of Food Science and Biotechnology, Kyonggi University) ;
  • Lee, Ho (Department of Food Science and Biotechnology, Kyonggi University)
  • Published : 2009.04.30

Abstract

A bacterial strain (Strain N-08) capable of extracellularly producing high level of non-reducing oligosaccharide (NR-OS) isolated from soil. The strain was identified phylogenetically by 16S rDNA sequence analysis and found to be very close to Arthrobacter crystallopoietes. The high production of NR-OS was observed in the basal culture medium containing maltose as a sole carbon source. The NR-OS in culture supernatant was purified by glucoamylase treatment and Dowex-1 (OH.) ion exchange chromatography and its structure was characterized. This oligosaccharide consisted of only glucose. Methylation analysis indicated that this fraction was composed mainly of non-reducing terminal glucopyranoside. Matrixassisted laser-induced/ionization time-of-flight (MALDI-TOF) and electrospray ionization-mass spectrometry (ESI-MS)/MS analyses suggested that this oligosaccharide comprised non-reducing disaccharide unit with 1,1-glucosidic linkage. When this disaccharide was analyzed by $^1H$-NMR and $^{13}C$-NMR, it gave the same signals with $\alpha$-D-glucopyranosyl-(1,1)-$\alpha$-Dglucopyranoside. These results indicated that the NR-OS produced by A. crystallopoietes N-08 was ${\alpha}1$,${\alpha}1$-trehalose. This is the first report of the trehalose which can be produced directly from maltose by A. crystallopoietes N-08.

Keywords

References

  1. French D. The Schardinger dextrins. Adv. Carbohyd. Chem. 12:189-260 (1957)
  2. Loftsson T, Brewster ME. Pharmaceutical applications of cyclodextrins. 1. Drug solubilization and stabilization. J. Pharm. Sci. 85: 1017-1025 (1996) https://doi.org/10.1021/js950534b
  3. Goubet I, Dahout C, Semon E, Guichard E, Le Quere JL, Voilley A. Competitive binding of aroma compounds by beta-cyclodextrin. J. Agr. Food Chem. 49: 5916-5922 (2001) https://doi.org/10.1021/jf0101049
  4. Tran CD, De Paoli Lacerda SH. Determination of binding constants of cyclodextrins in room-temperature ionic liquids by near-infrared spectrometry. Anal. Chem. 74: 5337-5341 (2002) https://doi.org/10.1021/ac020320w
  5. Wingler A. The function of trehalose biosynthesis in plants. Phytochemistry 60: 437-440 (2002) https://doi.org/10.1016/S0031-9422(02)00137-1
  6. Elbein AD, Pan YT, Pastuszak I, Carroll D. New insights on trehalose: A multifunctional molecule. Glycobiology 13: 17-27 (2003) https://doi.org/10.1093/glycob/cwg047
  7. Thevelein JM. Regulation of trehalose mobilization in fungi. Microbiol. Rev. 48: 42-59 (1984)
  8. Lillie SH, Pringle JR. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: Responses to nutrient limitation. J. Bacteriol. 143: 1384-1394 (1980)
  9. Kandror O, DeLeon A, Goldberg AL. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. P. Natl. Acad. Sci. USA 99: 9727-9732 (2002) https://doi.org/10.1073/pnas.142314099
  10. Kaushik JK, Bhat R. Why is trehalose an exceptional protein stabilizer? An analysis of the thermal stability of proteins in the presence of the compatible osmolyte trehalose. J. Biol. Chem. 278:26458-26465 (2003) https://doi.org/10.1074/jbc.M300815200
  11. Styrvold OB, Strom AR. Synthesis, accumulation, and excretion of trehalose in osmotically stressed Escherichia coli K-12 strains:Influence of amber suppressors and function of the periplasmic trehalase. J. Bacteriol. 173: 1187-1192 (1991) https://doi.org/10.1128/jb.173.3.1187-1192.1991
  12. Giaever HM, Styrvold OB, Kaasen I, Strom AR. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J. Bacteriol. 170: 2841-2849 (1988) https://doi.org/10.1128/jb.170.6.2841-2849.1988
  13. Nakada T, Maruta K, Mitzuzumi H, Kubota M, Chaen H, Sugimoto T, Kurimoto M, Tsujisaka Y. Purification and characterization of a novel enzyme, maltooligosyl trehalose trehalohydrolase, from Arthrobacter sp. Q36. Biosci. Biotech. Bioch. 59: 2215-2218 (1995) https://doi.org/10.1271/bbb.59.2215
  14. Nakada T, Maruta K, Mitzuzumi H, Tsukaki K, Kubota M, Chaen H, Sugimoto T, Kurimoto M, Tsujisaka Y. Purification and properties of a novel enzyme, maltooligosyl trehalose synthase, from Arthrobacter sp. Q36. Biosci. Biotech. Bioch. 59: 2210-2214 (1995) https://doi.org/10.1271/bbb.59.2210
  15. Roser B. Trehalose, a new approach to premium dried foods. Trends Food Sci. Tech. 7: 166-169 (1991)
  16. Maruta K, Nakada T, Kubota M, Chaen H, Sugimoto T, Kurimoto M, Tsujisaka Y. Formation of trehalose from maltooligosaccharides by a novel enzymatic system. Biosci. Biotech. Bioch. 59: 1829-1834 (1995) https://doi.org/10.1271/bbb.59.1829
  17. Paiva CL, Panek AD. Biotechnological applications of the disaccharide trehalose. Biotechnol. Annu. Rev. 2: 293-314 (1996) https://doi.org/10.1016/S1387-2656(08)70015-2
  18. Guo N, Puhlev I, Brown DR, Mansbridge J, Levine F. Trehalose expression confers desiccation tolerance on human cells. Nat. Biotechnol. 18: 168-171 (2000) https://doi.org/10.1038/72616
  19. Kim BY, Lee SY, Weon HY, Kwon SW, Go SJ, Park YK, Schumann P, Fritze D. Ureibacillus suwonensis sp. nov., isolated from cotton waste composts. Int. J. Syst. Evol. Micr. 56: 663-666 (2006) https://doi.org/10.1099/ijs.0.63703-0
  20. Kimura M. Estimation of evolutionary distances between homologous nucleotide sequences. P. Natl. Acad. Sci. USA 78: 454-458 (1981) https://doi.org/10.1073/pnas.78.1.454
  21. Saitou N, Nei M. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425 (1987)
  22. Felsenstein J. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39: 783-791 (1985) https://doi.org/10.2307/2408678
  23. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal. Chem. 28: 350-356 (1956) https://doi.org/10.1021/ac60111a017
  24. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72: 248-254 (1976) https://doi.org/10.1016/0003-2697(76)90527-3
  25. Somogyi M. Notes on sugar determination. J. Biol. Chem. 195: 19-23 (1952)
  26. Nelson N. A photometric adaptation of the Somogyi method for the determination of glucose. J. Biol. Chem. 153: 375-380 (1944)
  27. Jones TM, Albersheim P. A gas chromatography method for the determination of aldose and uronic acid constituents of plant cell wall polysaccharide. Plant Physiol. 49: 926-936 (1972) https://doi.org/10.1104/pp.49.6.926
  28. Lee CH, Oh SW, Kim IH, Kim YE, Hwang JH, Yu KW. Chemical properties and immunological activities of hot-water extract from leaves of saltwort. Food Sci. Biotechnol. 13: 167-171 (2004)
  29. Hakomori S. A rapid permethylation of glycolipid, and polysaccharide catalyzed by methylsulfinyl carbanion in dimethyl sulfoxide. J. Biochem. -Tokyo 55: 205-208 (1964)
  30. Choi HD, Seog HM, Choi IW, Lee CH, Shin KS. Molecular structure of β-glucans isolated from non-waxy and waxy barley. Food Sci. Biotechnol. 13: 744-748 (2004)
  31. Waeghe TJ, Darvill AG, McNeil M, Albersheim P. Determination by methylation analysis of the glycosyl linkage compositions of microgram quantities of complex carbohydrates. Carbohyd. Res. 123: 281-304 (1983) https://doi.org/10.1016/0008-6215(83)88484-5
  32. Sweet DP, Shapiro RH, Albersheim P. Quantitative analysis by various G.L.C. response-factor theories for partially methylated and partially ethylated alditol acetates. Carbohyd. Res. 40: 217-225 (1975) https://doi.org/10.1016/S0008-6215(00)82604-X
  33. Pauly M, Eberhard S, Albersheim P, Darvill A, York WS. Effects of the mur1 mutation on xyloglucans produced by suspension cultured Arabidopsis thaliana cells. Planta 214: 67-74 (2001) https://doi.org/10.1007/s004250100585
  34. Higashiyama T. Novel functions and applications of trehalose. Pure Appl. Chem. 74: 1263-1269 (2002) https://doi.org/10.1351/pac200274071263
  35. Richards AB, Krakowka S, Dexter LB, Schmid H, Wolterbeek APM, Waalkens-Berendsen DH, Shigoyuki A, Kurimoto M. Trehalose: A review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem. Toxicol. 40: 871-898 (2002) https://doi.org/10.1016/S0278-6915(02)00011-X
  36. Kizawa H, Miyazaki J, Yokota A, Kanegae Y, Miyagawa K, Sugiyama Y. Trehalose production by a strain of Micrococcus varians. Biosci. Biotech. Bioch. 59: 1522-1527 (1995) https://doi.org/10.1271/bbb.59.1522
  37. Lama L, Nicolaus B, Trincone A, Morzillo P, De Rosa M, Gambacorta A. Starch conversion with immobilized thermophilic archaebacterium Sulfolobus solfataricus. Biotechnol. Lett. 12: 431-432 (1990) https://doi.org/10.1007/BF01024398
  38. Nishimoto T, Nakano M, Nakada T, Chaen H, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y. Purification and properties of novel enzyme, trehalose synthase, from Pimelobacter sp. R48. Biosci. Biotech. Bioch. 60: 640-644 (1996) https://doi.org/10.1271/bbb.60.640
  39. Ohguchi M, Kubota N, Wada T, Yoshinaga K, Uritani M, Yagisawa M, Ohisgi K, Yamagishi M, Ohta T, Ishikawa K. Purification and properties of trehalose-synthesizing enzyme from Pseudomonas sp. F1. J. Ferment. Bioeng. 84: 358-360 (1997) https://doi.org/10.1016/S0922-338X(97)89260-4
  40. Kaasen I, McDougall J, Strom AR. Analysis of the otsBA operon for osmoregulatory trehalose synthesis in Escherichia coli and homology of the OtsA and OtsB proteins to the yeast trehalose-6-phosphate synthase/phosphatase complex. Gene 145: 9-15 (1994) https://doi.org/10.1016/0378-1119(94)90316-6
  41. Nishimoto T, Nakano M, Ikegami S, Chaen H, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y. Existence of a novel enzyme converting maltose into trehalose. Biosci. Biotech. Bioch. 59: 2189-2190 (1995) https://doi.org/10.1271/bbb.59.2189
  42. Marechal LR, Belocopitow E. Metabolism of trehalose in Euglena gracilis. I. Partial purification and some properties of trehalose phosphorylase. J. Biol. Chem. 247: 3223-3228 (1972)
  43. Kato M, Miura Y, Kettoku M, Shindo K, Iwamatsu A, Kobayashi K. Purification and characterization of new trehaloseproducing enzymes isolated from the hyperthermophilic archae, Sulfolobus solfataricus KM1. Biosci. Biotech. Bioch. 60: 546-550 (1996) https://doi.org/10.1271/bbb.60.546
  44. Nishimoto T, Nakada T, Chaen H, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y. Purification and characterization of a thermostable trehalose synthase from Thermus aquatics. Biosci. Biotech. Bioch. 60: 835-839 (1996) https://doi.org/10.1271/bbb.60.835
  45. Silva Z, Alarico S, Nobre A, Horlacher R, Marugg J, Boos W, Mingote AI, Da Costa MS. Osmotic adaptation of Thermus thermophilus RQ-1: Lesson from a mutant deficient in synthesis of trehalose. J. Bacteriol. 185: 5943-5952 (2003) https://doi.org/10.1128/JB.185.20.5943-5952.2003
  46. Chen YS, Lee GC, Shaw JF. Gene cloning, expression, and biochemical characterization of a recombinant trehalose synthase from Picrophilus torridus in Escherichia coli. J. Agr. Food Chem. 54: 7098-7104 (2006) https://doi.org/10.1021/jf060828q