Preventive Nutrition and Food Science

The Korean Society of Food Science and Nutrition (한국식품영양과학회)
권호 표지
DOI QR코드

DOI QR Code

Optimal Conditions and Substrate Specificity for Trehalose Production by Resting Cells of Arthrobacter crystallopoietes N-08

  • Seo, Yi-Seul (Department of Food Science and Biotechnology, Kyonggi University) ;
  • Shin, Kwang-Soon (Department of Food Science and Biotechnology, Kyonggi University)
  • Received : 2011.11.07
  • Accepted : 2011.12.15
  • Published : 2011.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Recently, we found that Arthrobacter crystallopoietes N-08 isolated from soil directly produces trehalose from maltose by a resting cell reaction. In this study, the optimal set of conditions and substrate specificity for the trehalose production using resting cells was investigated. Optimum temperature and pH of the resting cell reaction were $55^{\circ}C$ and pH 5.5, respectively, and the reaction was stable for two hours at $37{\sim}55^{\circ}C$ and for one hour at the wide pH ranges of 3~9. Various disaccharide substrates with different glycosidic linkages, such as maltose, isomaltose, cellobiose, nigerose, sophorose, and laminaribiose, were converted into trehalose-like spots in thin layer chromatography (TLC). These results indicated broad substrate specificity of this reaction and the possibility that cellobiose could be converted into other trehalose anomers such as ${\alpha},{\beta}$- and ${\beta},{\beta}$-trehalose. Therefore, the product after the resting cell reaction with cellobiose was purified by ${\beta}$-glucosidase treatment and Dowex-1 ($OH^-$) column chromatography and its structure was analyzed. Component sugar and methylation analyses indicated that this cellobiose-conversion product was composed of only non-reducing terminal glucopyranoside. MALDI-TOF and ESI-MS/MS analyses suggested that this oligosaccharide contained a non-reducing disaccharide unit with a 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)-${\alpha}$-D-glucopyranoside. These results suggest that cellobiose can be converted to ${\alpha},{\alpha}$-trehalose by the resting cells of A. crystallopoietes N-08.

Keywords

References

  1. Wingler A. 2002. The function of trehalose biosynthesis in plants. Phytochemistry 60: 437-440. https://doi.org/10.1016/S0031-9422(02)00137-1
  2. Elbein AD, Pan YT, Pastuszak I, Carroll D. 2003. New insights on trehalose: a multifunctional molecule. Glycobiology 13: 17-27.
  3. Thevelein JM. 1984. Regulation of trehalose mobilization in fungi. Microbiol Rev 48: 42-59.
  4. Lillie SH, Pringle JR. 1980. Reserve carbohydrate metabolism in Saccharomyces cerevisiae: responses to nutrient limitation. J Bacteriol 143: 1384-1394.
  5. Kandror O, DeLeon A, Goldberg AL. 2002. Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc Natl Acad Sci USA 99: 9727-9732. https://doi.org/10.1073/pnas.142314099
  6. Kaushik JK, Bhat R. 2003. 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. https://doi.org/10.1074/jbc.M300815200
  7. Higashiyama T. 2002. Novel functions and applications of trehalose. Pure Appl Chem 74: 1263-1269. https://doi.org/10.1351/pac200274071263
  8. Roser B. 1991. Trehalose, a new approach to premium dried foods. Trends Food Sci Technol 7: 166-169.
  9. Paiva CL, Panek AD. 1996. Biotechnological applications of the disaccharide trehalose. Biotechnol Annu Rev 2: 293-314. https://doi.org/10.1016/S1387-2656(08)70015-2
  10. Guo N, Puhlev I, Brown DR, Mansbridge J, Levine F. 2000. Trehalose expression confers desiccation tolerance on human cells. Nat Biotechnol 18: 168-171. https://doi.org/10.1038/72616
  11. Giaever HM, Styrvold OB, Kaasen I, Strom AR. 1988. Biochemical and genetic characterization of osmoregulatory trehalose synthesis in Escherichia coli. J Bacteriol 170: 2841-2849. https://doi.org/10.1128/jb.170.6.2841-2849.1988
  12. Styrvold OB, Strom AR. 1991. 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. https://doi.org/10.1128/jb.173.3.1187-1192.1991
  13. Nakada T, Maruta K, Mitzuzumi H, Tsukaki K, Kubota M, Chaen H, Sugimoto T, Kurimoto M, Tsujisaka Y. 1995. Purification and properties of a novel enzyme, maltooligosyl trehalose synthase, from Arthrobacter sp. Q36. Biosci Biotechnol Biochem 59: 2210-2214. https://doi.org/10.1271/bbb.59.2210
  14. Nakada T, Maruta K, Mitzuzumi H, Kubota M, Chaen H, Sugimoto T, Kurimoto M, Tsujisaka Y. 1995. Purification and characterization of a novel enzyme, maltooligosyl trehalose trehalohydrolase, from Arthrobacter sp. Q36. Biosci Biotechnol Biochem 59: 2215-2218. https://doi.org/10.1271/bbb.59.2215
  15. Bae BS, Shin KS, Lee H. 2009. Structural characterization of non-reducing oligosaccharides produced by Arthrobacter crystallopoietes N-08. Food Sci Biotechnol 18: 519-525.
  16. Miller GL. 1959. Use of dinitrosalicylic acid reagent for determination of reducing sugar. Anal Chem 31: 426-428. https://doi.org/10.1021/ac60147a030
  17. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Anal Chem 28: 350-356. https://doi.org/10.1021/ac60111a017
  18. Bradford MM. 1976. 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. https://doi.org/10.1016/0003-2697(76)90527-3
  19. Somogyi M. 1952. Notes on sugar determination. J Biol Chem 195: 19-23.
  20. Nelson N. 1944. A photometric adaptation of the Somogyi method for the determination of glucose. J Biol Chem 153: 375-380.
  21. Jones TM, Albersheim P. 1972. A gas chromatography method for the determination of aldose and uronic acid constituents of plant cell wall polysaccharide. Plant Physiol 49: 926-936. https://doi.org/10.1104/pp.49.6.926
  22. Lee CH, Oh SW, Kim IH, Kim YE, Hwang JH, Yu KW. 2004. Chemical properties and immunological activities of hot-water extract from leaves of saltwort. Food Sci Biotechnol 13: 167-171.
  23. Hakomori S. 1964. A rapid permethylation of glycolipid, and polysaccharide catalyzed by methylsulfinyl carbanion in dimethyl sulfoxide. J Biochem 55: 205-208.
  24. Choi HD, Seog HM, Choi IW, Lee CH, Shin KS. 2004. Molecular structure of $\beta$ -glucans isolated from non-waxy and waxy barley. Food Sci Biotechnol 13: 744-748.
  25. Waeghe TJ, Darvill AG, McNeil M, Albersheim P. 1983. Determination by methylation analysis of the glycosyl linkage compositions of microgram quantities of complex carbohydrates. Carbohydr Res 123: 281-304. https://doi.org/10.1016/0008-6215(83)88484-5
  26. Sweet DP, Shapiro RH, Albersheim P. 1975. Quantitative analysis by various G.L.C. response-factor theories for partially methylated and partially ethylated alditol acetates. Carbohydr Res 40: 217-225. https://doi.org/10.1016/S0008-6215(00)82604-X
  27. Pauly M, Eberhard S, Albersheim P, Darvill A, York WS. 2001. Effects of the mur1 mutation on xyloglucans produced by suspension cultured Arabidopsis thaliana cells. Planta 214: 67-74. https://doi.org/10.1007/s004250100585
  28. Nishimoto T, Nakano M, Nakada T, Chaen H, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y. 1996. Purification and properties of novel enzyme, trehalose synthase, from Pimelobacter sp. R48. Biosci Biotechnol Biochem 60: 640-644. https://doi.org/10.1271/bbb.60.640
  29. Nishimoto T, Nakada T, Chaen H, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y. 1996. Purification and characterization of a thermostable trehalose synthase from Thermos aquaticus. Biosci Biotechnol Biochem 60: 835-839. https://doi.org/10.1271/bbb.60.835
  30. Di Lernia I, Morana A, Ottombrino A, Fusco S, Rossi M, De Rosa M. 1998. Enzymes from Sulfolobus shibatae for the production of trehalose and glucose from starch. Extremophiles 2: 409-416. https://doi.org/10.1007/s007920050086
  31. Ohguchi M, Kubota N, Wada T, Yoshinaga K, Uritani M, Yagisawa M, Ohisgi K, Yamagishi M, Ohta T, Ishikawa K. 1997. Purification and properties of trehalose-synthesizing enzyme from Pseudomonas sp. F1. J Ferment Bioeng 84: 358-360. https://doi.org/10.1016/S0922-338X(97)89260-4
  32. Vanderghem C, Boquel P, Blecker C, Paquot M. 2010. A multistage process to enhance cellobiose production from cellulosic materials. Appl Biochem Biotechnol 160: 2300-2307. https://doi.org/10.1007/s12010-009-8724-7
  33. Richards AB, Krakowka S, Dexter LB, Schmid H, Wolterbeek APM, Waalkens-berendsen DH, Shigoyuki A, Kurimoto M. 2002. Trehalose: a review of properties, history of use and human tolerance, and results of multiple safety studies. Food Chem Toxicol 40: 871-898. https://doi.org/10.1016/S0278-6915(02)00011-X