Identification and characterization of a novel Terrabacter ginsenosidimutans sp. nov. β-glucosidase that transforms ginsenoside Rb1 into the rare gypenosides XVII and LXXV

Applied and Environmental Microbiology

Volumn 76, Issue 17, 2010, Pages 5827-5836

  An, Dong Shan ^a   Cui, Chang Hao ^b   Lee, Hyung Gwan ^b   Wang, Liang ^b   Kim, Sun Chang ^b   Lee, Sung Taik ^b   Jin, Fengxie ^c   Yu, Hongshan ^c   Chin, Young Won ^a   Lee, Hyeong Kyu ^a   Im, Wan Taek ^b   Kim, Song Gun ^a  

^a Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

^b Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^c DALIAN POLYTECHNIC UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

20-PROTOPANAXADIOL; APPARENT K; E. COLI; GINSENOSIDE RB1; GINSENOSIDES; GLUCOPYRANOSIDE; GLUCOSIDASE; GLYCOSIDE HYDROLASES; GYPENOSIDES; NOVEL STRAINS;

CATALYSIS; CLONING; ENZYMES; ESCHERICHIA COLI; GLUCOSE; PLANTS (BOTANY);

PHARMACODYNAMICS;

BACTERIAL DNA; BACTERIAL PROTEIN; BETA GLUCOSIDASE; CARDIOLIPIN SYNTHASE; GINSENOSIDE; GINSENOSIDE RB 1; GYPENOSIDE; MEMBRANE PROTEIN; PHOSPHOTRANSFERASE; PLANT EXTRACT;

BACTERIUM; CATALYSIS; CHEMICAL COMPOSITION; CLONE; ENZYME ACTIVITY; EXPERIMENTAL STUDY; HYDROLYSIS; PH;

ACTINOMYCETALES; ARTICLE; BIOTRANSFORMATION; CHEMICAL STRUCTURE; CHEMISTRY; CLUSTER ANALYSIS; DNA SEQUENCE; ENZYME SPECIFICITY; ENZYMOLOGY; ESCHERICHIA COLI; GENETICS; GINSENG; GYNOSTEMMA; ISOLATION AND PURIFICATION; KINETICS; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE HOMOLOGY;

ACTINOMYCETALES; BACTERIAL PROTEINS; BETA-GLUCOSIDASE; BIOTRANSFORMATION; CLONING, MOLECULAR; CLUSTER ANALYSIS; DNA, BACTERIAL; ESCHERICHIA COLI; GINSENOSIDES; GYNOSTEMMA; KINETICS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; PANAX; PHYLOGENY; PLANT EXTRACTS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, NUCLEIC ACID; SOIL MICROBIOLOGY; SUBSTRATE SPECIFICITY; TRANSFERASES (OTHER SUBSTITUTED PHOSPHATE GROUPS);

ESCHERICHIA COLI; PANAX GINSENG; TERRABACTER;

EID: 77956563577     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00106-10     Document Type: Article

References (48)

1. Akao, T., H. Kida, M. Kanaoka, M. Hattori, and K. Kobashi. 1998. Intestinal bacterial hydrolysis is required for the appearance of compound K in rat plasma after oral administration of ginsenoside Rb1 from Panax ginseng. J. Pharm. Pharmacol. 50:1155-1160. (Pubitemid 28488135)
2. Bae, E. A., M. J. Han, E. J. Kim, and D. H. Kim. 2004. Transformation of ginseng saponins to ginsenoside Rh2 by acids and human intestinal bacteria and biological activities of their transformants. Arch. Pharm. Res. 27:61-67.
3. Buck, J. D. 1982. Nonstaining (KOH) method for determination of Gram reactions of marine bacteria. Appl. Environ. Microbiol. 44:992-993.
4. Cheng, L. Q., J. R. Na, M. K. Kim, M. H. Bang, and D. C. Yang. 2007. Microbial conversion of ginsenoside Rb1 to minor ginsenoside F2 and gypenoside XVII by Intrasporangium sp. GS603 isolated from soil. J. Microbiol. Biotechnol. 17:1937-1943.
5. Christensen, L. P. 2009. Ginsenosides: chemistry, biosynthesis, analysis, and potential health effects. Adv. Food Nutr. Res. 55:1-99.
6. Cleland, W. W. 1979. Statistical analysis of enzyme kinetic data. Methods Enzymol. 63:103-138.
7. Collins, M. D. 1985. Analysis of isoprenoid quinones. Methods Microbiol. 18:329-366.
8. Ezaki, T., Y. Hashimoto, and E. Yabuuchi. 1989. Fluorometric deoxyribonucleic acid-deoxyribonucleic acid hybridization in microdilution wells as an alternative to membrane filter hybridization in which radioisotopes are used to determine genetic relatedness among bacterial strains. Int. J. Syst. Bacteriol. 39:224-229.
9. Felsenstein, J. 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783-791.
10. Fitch, W. M. 1971. Toward defining the course of evolution: minimum change for a specific tree topology. Syst. Zool. 20:406-416.
11. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
12. Harvey, A. J., M. Hrmova, R. De Gori, J. N. Varghese, and G. B. Fincher. 2000. Comparative modeling of the three-dimensional structures of family 3 glycoside hydrolases. Proteins 41:257-269.
13. Henrissat, B., and G. Davies. 1997. Structural and sequence-based classification of glycoside hydrolases. Curr. Opin. Struct. Biol. 7:637-644.
14. Kim, B. H., S. Y. Lee, H. J. Cho, S. N. You, Y. J. Kim, Y. M. Park, J. K. Lee, M. Y. Baik, C. S. Park, and S. C. Ahn. 2006. Biotransformation of Korean Panax ginseng by Pectinex. Biol. Pharm. Bull. 29:2472-2478.
15. 2+ channel-mediated cell death in rat cortical neurons. Biochem. Biophys. Res. Commun. 365:399-405.
16. Kim, S. J., C. M. Lee, M. Y. Kim, Y. S. Yeo, S. H. Yoon, H. C. Kang, and B. S. Koo. 2007. Screening and characterization of an enzyme with β-glucosidase activity from environmental DNA. J. Microbiol. Biotechnol. 17:905-912.
17. Kim, W. Y., J. M. Kim, S. B. Han, S. K. Lee, N. D. Kim, M. K. Park, C. K. Kim, and J. H. Park. 2000. Steaming of ginseng at high temperature enhances biological activity. J. Nat. Prod. 63:1702-1704.
18. Kim, Y. S., C. S. Park, and D. K. Oh. 2006. Lactulose production from lactose and fructose by a thermostable β-galactosidase from Sulfolobus solfataricus. Enzyme Microb. Technol. 39:903-908.
19. Kimura, M. 1983. The neutral theory of molecular evolution. Cambridge University Press, Cambridge, United Kingdom.
20. Ko, S. R., Y. Suzuki, K. J. Choi, and Y. H. Kim. 2000. Enzymatic preparation of genuine prosapogenin, 20 (S)-ginsenoside Rh1, from ginsenosides Re and Rg1. Biosci. Biotechnol. Biochem. 64:2739-2743.
21. Komagata, K., and K. Suzuki. 1987. Lipid and cell-wall analysis in bacterial systematics. Methods Microbiol. 19:161-207.
22. Lee, J.-E., J. P. Seo, D. W. Lee, Y. H. Ko, and S. D. Lee. 2008. Terrabacter lapilli sp. nov., a novel actinomycete isolated from stone. Int. J. Syst. Evol. Microbiol. 58:1084-1088.
23. Lee, S. J., J. H. Sung, C. K. Moon, and B. H. Lee. 1999. Antitumor activity of a novel ginseng saponin metabolite in human pulmonary adenocarcinoma cells resistant to cisplatin. Cancer Lett. 144:39-43.
24. Margolles, A., and C. G. de Los Reyes-Gavilan. 2003. Purification and functional characterization of a novel a-L-arabinofuranosidase from Bifidobacterium longum B667. Appl. Environ. Microbiol. 69:5096-5103.
25. Mesbah, M., U. Premachandran, and W. B. Whitman. 1989. Precise measurement of the G+C content of deoxyribonucleic acid by high-performance liquid chromatography. Int. J. Syst. Bacteriol. 39:159-167.
26. Minnikin, D. E., A. G. O'Donnell, M. Goodfellow, G. Alderson, M. Athalye, K. Schaal, and J. H. Parlett. 1984. An integrated procedure for the extraction of isoprenoid quinones and polar lipids. J. Microbiol. Methods 2:233-241.
27. Nagai, M., T. Ando, N. Tanaka, O. Tanaka, and S. Shibata. 1972. Chemical studies on the oriental plant drugs. XXVIII. Saponins and sapogenins of ginseng: stereochemistry of the sapogenin of ginsenoside Rb1, Rb2 and Rc. Chem. Pharm. Bull. 20:1212-1216.
28. Noh, K. H., J. W. Son, H. J. Kim, and D. K. Oh. 2009. Ginsenoside compound K production from ginseng root extract by a thermostable betaglycosidase from Sulfolobus solfataricus. Biosci. Biotechnol. Biochem. 73:316-321.
29. Park, J. D., D. K. Rhee, and Y. H. Lee. 2005. Biological activities and chemistry of saponins from Panax ginseng C. A. Meyer. Phytochem. Rev. 4:159-175.
30. Park, J. H. 2004. Sun ginseng-a new processed ginseng with fortified activity. Food Ind. Nutr. 9:23-27.
31. Rhule, A., B. Rase, J. R. Smith, and D. M. Shepherd. 2008. Toll-like receptor ligand-induced activation of murine DC2.4 cells is attenuated by Panax notoginseng. J. Ethnopharmacol. 116:179-186.
32. Saitou, N., and M. Nei. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
33. Sasser, M. 1990. Identification of bacteria by gas chromatography of cellular fatty acids. Technical note 101. Microbial ID, Newark, DE.
34. Shin, H. Y., S. Y. Park, J. H. Sung, and D. H. Kim. 2003. Purification and characterization of Zα-L-arabinopyranosidase and α-L- arabinofuranosidase from Bifidobacterium breve K-110, a human intestinal anaerobic bacterium metabolizing ginsenoside Rb2 and Rc. Appl. Environ. Microbiol. 69:7116-7123.
35. Smibert, R. M., and N. R. Krieg. 1994. Phenotypic characterization, p. 607-654. In P. Gerhardt, R. G. E. Murray, W. A. Wood, and N. R. Krieg (ed.), Methods for general and molecular microbiology. ASM Press, Washington, DC.
36. Tamura, K., J. Dudley, M. Nei, and S. Kumar. 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24:1596-1599.
37. Tawab, M. A., U. Bahr, M. Karas, M. Wurglics, and M. Schubert-Zsilavecz. 2003. Degradation of ginsenosides in humans after oral administration. Drug Metab. Dispos. 31:1065-1071.
38. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The CLUSTAL X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
39. Wang, W., E. R. Rayburn, M. Hao, Y. Zhao, D. L. Hill, R. Zhang, and H. Wang. 2008. Experimental therapy of prostate cancer with novel natural product anti-cancer ginsenosides. Prostate 68:809-819.
40. Wayne, L. G., D. J. Brenner, and R. R. Colwell. 1987. Report of the ad hoc committee on reconciliation of approaches to bacterial systematics. Int. J. Syst. Bacteriol. 37:463-464.
41. Weon, H.-Y., P. Schumann, R. M. Kroppenstedt, B.-Y. Kim, J. Song, S.-W. Kwon, S.-J. Go, and E. Stackebrandt. 2007. Terrabacter aerolatus sp. nov., isolated from an air sample. Int. J. Syst. Evol. Microbiol. 57:2106-2109.
42. Weon, H. Y., J. A. Son, S. H. Yoo, B. Y. Kim, S. W. Kwon, P. Schumann, R. Kroppenstedt, and E. Stackebrandt. 2010. Terrabacter aeriphilus sp. nov., isolated from an air sample. Int. J. Syst. Evol. Microbiol. 60:1130-1134.
43. Wu, J. Y., B. H. Gardner, C. I. Murphy, J. R. Seals, C. R. Kensil, and J. Recchia. 1992. Saponin adjuvant enhancement of antigen-specific immune responses to an experimental HIV-1 vaccine. J. Immunol. 148:1519-1525.
44. Xu, Q. F., X. L. Fang, and D. F. Che. 2003. Pharmacokinetics and bioavailability of ginsenoside Rb1 and Rg1 from Panax notoginseng in rats. J. Ethnopharmacol. 84:187-192.
45. Yan, Q., X. W. Zhou, W. Zhou, X. W. Li, M. Q. Feng, and P. Zhou. 2008. Purification and properties of a novel beta-glucosidase, hydrolyzing ginsenoside Rb1 to CK, from Paecilomyces Bainier. J. Microbiol. Biotechnol. 18:1081-1089.
46. Yoon, J. H., S. Park, S. J. Kang, Y. T. Jung, and W. Kim. 2009. Terrabacter terrigena sp. nov., isolated from soil. Int. J. Syst. Evol. Microbiol. 59:2798-2802.
47. Yoshikawa, K., M. Arimitsu, K. Kishi, T. Takemoto, and S. Arihara. 1987. Studies on the constituents of Cucurbitaceae plants. XVIII. On the saponin constituents of Gynostemma pentaphyllum Makino. Yakugaku Zasshi 107:361-366. (In Japanese.) (Pubitemid 17097440)
48. Yun, T.-K., Y.-S. Lee, Y. H. Lee, S. I. Kim, and H. Y. Yun. 2001. Cancer chemopreventive compounds of red ginseng produced from Panax ginseng C. A. Meyer. J. Ginseng Res. 25:107-111.