Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
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Characterization of Ribose-5-Phosphate Isomerase B from Newly Isolated Strain Ochrobactrum sp. CSL1 Producing ʟ-Rhamnulose from ʟ-Rhamnose

  • Shen, Min (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology) ;
  • Ju, Xin (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology) ;
  • Xu, Xinqi (Fujian Key Laboratory of Marine Enzyme Engineering, Fuzhou University) ;
  • Yao, Xuemei (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology) ;
  • Li, Liangzhi (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology) ;
  • Chen, Jiajia (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology) ;
  • Hu, Cuiying (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology) ;
  • Fu, Jiaolong (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology) ;
  • Yan, Lishi (School of Chemistry, Biology, and Material Engineering, Suzhou University of Science and Technology)
  • Received : 2018.02.14
  • Accepted : 2018.04.13
  • Published : 2018.07.28
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Abstract

In this study, we attempted to find new and efficient microbial enzymes for producing rare sugars. A ribose-5-phosphate isomerase B (OsRpiB) was cloned, overexpressed, and preliminarily purified successfully from a newly screened Ochrobactrum sp. CSL1, which could catalyze the isomerization reaction of rare sugars. A study of its substrate specificity showed that the cloned isomerase (OsRpiB) could effectively catalyze the conversion of $\text\tiny{L}$-rhamnose to $\text\tiny{L}$-rhamnulose, which was unconventional for RpiB. The optimal reaction conditions ($50^{\circ}C$, pH 8.0, and 1 mM $Ca^{2+}$) were obtained to maximize the potential of OsRpiB in preparing $\text\tiny{L}$-rhamnulose. The catalytic properties of OsRpiB, including $K_m$, $k_{cat}$, and catalytic efficiency ($k_{cat}/K_m$), were determined as 43.47 mM, $129.4sec^{-1}$, and 2.98 mM/sec. The highest conversion rate of $\text\tiny{L}$-rhamnose under the optimized conditions by OsRpiB could reach 26% after 4.5 h. To the best of our knowledge, this is the first successful attempt of the novel biotransformation of $\text\tiny{L}$-rhamnose to $\text\tiny{L}$-rhamnulose by OsRpiB biocatalysis.

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References

  1. Zhang W, Zhang T, Jiang B, Mu W. 2017. Enzymatic approaches to rare sugar production. Biotechnol. Adv. 35: 267-274. https://doi.org/10.1016/j.biotechadv.2017.01.004
  2. Shompoosang S, Yoshihara A, UechiK, Asada Y, Morimoto K. 2016. Novel process for producing 6-deoxy monosaccharides from L-fucose by coupling and sequential enzymatic method. J. Biosci. Bioeng. 121: 1-6. https://doi.org/10.1016/j.jbiosc.2015.04.017
  3. Beerens K, Desmet T, Soetaert W. 2012. Enzymes for the biocatalytic production of rare sugars. J. Ind. Microbiol. Biotechnol. 39: 823-834. https://doi.org/10.1007/s10295-012-1089-x
  4. Chen Z, Xu W, Zhang W, Zhang T, Jiang B, Mu W. 2018. Characterization of a thermostable recombinant L-rhamnose isomerase from Caldicellulosiruptor obsidiansis OB47 and its application for the production of L-fructose and L-rhamnulose. J. Sci. Food. Agric. 98: 2184-2193. https://doi.org/10.1002/jsfa.8703
  5. Wen L, Zang L, Huang K, Li S, Wang R, Wang PG. 2016. Efficient enzymatic synthesis of L-rhamnulose and L-fuculose. Bioorg. Med. Chem. Lett. 26: 969-972. https://doi.org/10.1016/j.bmcl.2015.12.051
  6. Shompoosang S, Yoshihara A, Uechi K, Asada Y, Morimoto K. 2014. Enzymatic production of three 6-deoxy-aldohexoses from L-rhamnose. Biosci. Biotechnol. Biochem. 78: 317-325. https://doi.org/10.1080/09168451.2014.878217
  7. Kim YS, Shin KC, Lim YR, Oh DK. 2013. Characterization of a recombinant L-rhamnose isomerase from Dictyoglomus turgidum and its application for L-rhamnulose production. Biotechnol. Lett. 35: 259-264. https://doi.org/10.1007/s10529-012-1069-2
  8. Park CS, Yeom SJ, Kim HJ, Lee SH, Lee JK, Kim SW, Oh DK. 2007. Characterization of ribose-5-phosphate isomerase of Clostridium thermocellum producing D-allose from D-psicose. Biotechnol. Lett. 29: 1387-1391. https://doi.org/10.1007/s10529-007-9393-7
  9. Lee TE, Shin KC, Oh DK. 2018. Biotransformation of fructose to allose by one-pot reaction using Flavonifractor plautii D-allulose 3-epimerase and Clostridium thermocellumribose 5-phosphate isomerase. J. Microbiol. Biotechnol. 28: 418-424. https://doi.org/10.4014/jmb.1709.09044
  10. Yeom SJ, Kim BN, Park CS, Oh DK. 2010. Substrate specificity of ribose-5-phosphate isomerases from Clostridium difficile and Thermotoga maritima. Biotechnol. Lett. 32: 829-835. https://doi.org/10.1007/s10529-010-0224-x
  11. Park CS, Yeom SJ, Lim YR, Kim YS, Oh DK. 2011. Substrate specificity of a recombinant ribose-5-phosphate isomerase from Streptococcus pneumoniae and its application in the production of L-lyxose and L-tagatose. World. J. Microbiol. Biotechnol. 27: 743-750. https://doi.org/10.1007/s11274-010-0511-7
  12. Morimoto K, Terami Y, Maeda Y, Yoshihara A, Takata G, Izumori K. 2013. Cloning and characterization of the L-ribose isomerase gene from Cellulomonas parahominis MB426. J. Biosci. Bioeng. 115: 377-381. https://doi.org/10.1016/j.jbiosc.2012.10.021
  13. 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
  14. Dische Z, Borenfreuod E. 1951. A new spectrophotometric method for the detection and determination of keto sugars and trioses. J. Biol. Chem. 192: 583-587.
  15. Mizanur RM, Takada G, Izumori K. 2001. Cloning and characterization of a novel gene encoding L-ribose isomerase from Acinetobacter sp. strain DL-28 in Escherichia coli. Biochim. Biophys. Acta 1521: 141-145. https://doi.org/10.1016/S0167-4781(01)00290-1
  16. Edwards TE, Abramov AB, Smith ER, Baydo RO, Leonard JT, Leibly DJ, et al. 2011. Structural characterization of a ribose- 5-phosphate isomerase B from the pathogenic fungus Coccidioides immitis. BMC Struct. Biol. 11: 39. https://doi.org/10.1186/1472-6807-11-39
  17. Kaur PK, Tripathi N, Desale J, Neelagiri S, Yadav S, Bharatam PV, et al. 2016. Mutational and structural analysis of conserved residues in ribose-5-phosphate isomerase B from Leishmania donovani: role in substrate recognition and conformational stability. PLoS One 11: e0150764. https://doi.org/10.1371/journal.pone.0150764
  18. Essenberg MK, Cooper RA. 1975. Two ribose-5-phosphate isomerases from Escherichia coli K12: partial characterization of the enzymes and consideration of their possible physiological roles. Eur. J. Biochem. 55: 323-332. https://doi.org/10.1111/j.1432-1033.1975.tb02166.x
  19. Yeom SJ, Seo ES, Kim YS, Oh DK. 2011. Increased D-allose production by the R132E mutant of ribose-5-phosphate isomerase from Clostridium thermocellum. Appl. Microbiol. Biotechnol. 89: 1859-1866. https://doi.org/10.1007/s00253-010-3026-0
  20. Feng Z, Mu W, Jiang B. 2013. Characterization of ribose-5- phosphate isomerase converting D-psicose to D-allose from Thermotoga lettingae TMO. Biotechnol. Lett. 35: 719-724. https://doi.org/10.1007/s10529-013-1136-3
  21. Badia J, Gimenez R, Baldoma L, Barnes E, Fessner WD, Aguilar J. 1991. L-Lyxose metabolism employs the L-rhamnose pathway in mutant cells of Escherichia coli adapted to grow on L-lyxose. J. Bacteriol. 173: 5144-5150. https://doi.org/10.1128/jb.173.16.5144-5150.1991
  22. Leang K, Takada G, Fukai Y, Morimoto K, Granstrom TB, Izumori K. 2004. Novel reactions of L-rhamnose isomerase from Pseudomonas stutzeri and its relation with D-xylose isomerase via substrate specificity. Biochim. Biophys. Acta 1674: 68-77. https://doi.org/10.1016/j.bbagen.2004.06.003
  23. Poonperm W, Takata G, Okada H, Morimoto K, Granström TB, Izumori K. 2007. Cloning, sequencing, overexpression and characterization of L-rhamnose isomerase from Bacillus pallidus Y25 for rare sugar production. Appl. Microbiol. Biotechnol. 76: 1297-1307. https://doi.org/10.1007/s00253-007-1109-3
  24. Park CS, Yeom SJ, Lim YR, Kim YS, Oh DK. 2010. Characterization of a recombinant thermostable L-rhamnose isomerase from Thermotoga maritima ATCC 43589 and its application in the production of L-lyxose and L-mannose. Biotechnol. Lett. 32: 1947-1953. https://doi.org/10.1007/s10529-010-0385-7
  25. Lin CJ, Tseng WC, Fang TY. 2011. Characterization of a thermophilic L-rhamnose isomerase from Caldicellulosiruptor saccharolyticus ATCC 43494. J. Agric. Food Chem. 59: 8702-8708. https://doi.org/10.1021/jf201428b
  26. Lin CJ, Tseng WC, Lin TH, Liu SM, Tzou WS, Fang TY. 2010. Characterization of a thermophilic L-rhamnose isomerase from Thermoanaerobacterium saccharolyticum NTOU1. J. Agric. Food Chem. 58: 10431-10436. https://doi.org/10.1021/jf102063q
  27. Prabhu P, Doan TT, Jeya M, Kang LW, Lee JK. 2011. Cloning and characterization of a rhamnose isomerase from Bacillus halodurans. Appl. Microbiol. Biotechnol. 89: 635-644. https://doi.org/10.1007/s00253-010-2844-4
  28. Jung J, Kim J, Yeom S, Ahn Y, Oh D, Kang L. 2011. Crystal structure of Clostridium thermocellum ribose-5-phosphate isomerase B reveals properties critical for fast enzyme kinetics. Appl. Microbiol. Biotechnol. 90: 517-527. https://doi.org/10.1007/s00253-011-3095-8
  29. Whitaker RD, Cho Y, Cha J, Carrell HL, Glusker JP, Karplus PA, et al. 1995. Probing the roles of active site residues in D-xylose isomerase. J. Biol. Chem. 270: 22895-22906. https://doi.org/10.1074/jbc.270.39.22895
  30. Kovalevsky AY, Hanson L, Fisher SZ, Mustyakimov M, Mason SA, Forsyth VT, et al. 2010. Metal ion roles and the movement of hydrogen during reaction catalyzed by D-xylose isomerase: a joint x-ray and neutron diffraction study. Structure 18: 688-699. https://doi.org/10.1016/j.str.2010.03.011

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