Applied Microbiology and Biotechnology

, Volume 102, Issue 5, pp 2051–2062 | Cite as

d-lyxose isomerase and its application for functional sugar production

  • Jiawei Huang
  • Ziwei Chen
  • Wenli Zhang
  • Tao Zhang
  • Wanmeng Mu
Mini-Review
  • 68 Downloads

Abstract

Functional sugars have attracted attention because of their wide application prospects in the food, cosmetics, and pharmaceutical industries in recent decades. Compared with complex chemical synthesis, enzymatic methods of creating functional sugars, characterized by high specificity, moderate reaction conditions, and sustainability, are favored. d-lyxose isomerase (d-LI, EC 5.3.1.15), an important aldose-ketose isomerase, catalyzes the reverse isomerization reaction between d-xylulose and d-lyxose, as well as d-fructose and d-mannose. d-LI has drawn researchers’ attention due to its broad substrate specificity and high potential for enzymatic production of some functional sugars such as d-xylulose, d-mannose, and d-ribose. In this article, an overview of recent advances in the biochemical properties of various d-LIs is explored in detail. Structural analysis, active site identification, and catalytic mechanisms are also provided. Additionally, the applications of d-LIs for functional sugar production, including d-lyxose, d-mannose, and l-ribose, are reviewed in detail in this paper.

Keywords

d-lyxose isomerase d-lyxose Substrate specificity Functional sugar 

Notes

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Supplementary material

253_2018_8746_MOESM1_ESM.pdf (488 kb)
ESM 1 (PDF 487 kb)

References

  1. Ahmed Z, Sasahara H, Bhuiyan SH, Saiki T, Shimonishi T, Takada G, Izumori K (1999) Production of D-lyxose from D-glucose by microbial and enzymatic reactions. J Biosci Bioeng 88(6):676–678.  https://doi.org/10.1016/S1389-1723(00)87100-5 CrossRefPubMedGoogle Scholar
  2. Anderson RL, Allison DP (1965) Purification and characterization of D-lyxose isomerase. J Biol Chem 240(8):2367–2372PubMedGoogle Scholar
  3. Bhosale SH, Rao MB, Deshpande VV (1996) Molecular and industrial aspects of glucose isomerase. Microbiol Rev 60(2):280–300PubMedPubMedCentralGoogle Scholar
  4. Bicas JL, Silva JC, Pastore GM (2010) Biotechnological production of bioflavors and functional sugars. Cienc Tecnol Aliment 30(1):7–18CrossRefGoogle Scholar
  5. Bock K, Meldal M, Meyer B, Wiebe L (1983) Isomerization of D-glucose with glucose-isomerase. A mechanistic study. Acta Chem Scand 37(2):101–108CrossRefGoogle Scholar
  6. Bosshart A, Hee CS, Bechtold M, Schirmer T, Panke S (2015) Directed divergent evolution of a thermostable D-tagatose epimerase towards improved activity for two hexose substrates. Chembiochem 16(4):592–601.  https://doi.org/10.1002/cbic.201402620 CrossRefPubMedGoogle Scholar
  7. Bosshart A, Panke S, Bechtold M (2013) Systematic optimization of interface interactions increases the thermostability of a multimeric enzyme. Angew Chem Int Edit 125(37):9855–9858CrossRefGoogle Scholar
  8. Chen F, Wei X, Tao Z, Zhou L, Bo J, Mu W (2015) Engineering of Alicyclobacillus hesperidum l-arabinose isomerase for improved catalytic activity and reduced pH optimum using random and site-directed mutagenesis. Appl Biochem Biotechnol 177(7):1480–1492CrossRefGoogle Scholar
  9. Chen F, Zhao J, Xiong F, Xie B, Zhang P (2007) An improved synthesis of a key intermediate for (+)-biotin from D-mannose. Carbohydr Res 342(16):2461–2464.  https://doi.org/10.1016/j.carres.2007.06.029 CrossRefPubMedGoogle Scholar
  10. Chen Z, Xu W, Zhang W, Zhang T, Jiang B, Mu W (2017) 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.  https://doi.org/10.1002/jsfa.8703
  11. Cho EA, Lee DW, Cha YH, Lee SJ, Jung HC, Pan JG, Pyun YR (2007) Characterization of a novel D-lyxose isomerase from Cohnella laevoribosii RI-39 sp. nov. J Bacteriol 189(5):1655–1663.  https://doi.org/10.1128/JB.01568-06 CrossRefPubMedGoogle Scholar
  12. Choi JG, Hong SH, Kim YS, Kim KR, Oh DK (2012) Characterization of a recombinant thermostable D-lyxose isomerase from Dictyoglomus turgidum that produces D-lyxose from D-xylulose. Biotechnol Lett 34(6):1079–1085.  https://doi.org/10.1007/s10529-012-0874-y CrossRefPubMedGoogle Scholar
  13. De LP, Seta N (2009) The clinical spectrum of phosphomannose isomerase deficiency, with an evaluation of mannose treatment for CDG-Ib. BBA-M Basis Dis 1792(9):841–843CrossRefGoogle Scholar
  14. Friedman M (1996) Food browning and its prevention: an overview. J Agric Food Chem 44(3):631–653.  https://doi.org/10.1021/jf950394r CrossRefGoogle Scholar
  15. Harding MM (2006) Small revisions to predicted distances around metal sites in proteins. Acta Crystallogr 62(6):678–682Google Scholar
  16. Hartley BS, Hanlon N, Jackson RJ, Rangarajan M (2000) Glucose isomerase: insights into protein engineering for increased thermostability. BBA Protein Struct Mol Enzym 1543(2):294–335.  https://doi.org/10.1016/S0167-4838(00)00246-6 CrossRefGoogle Scholar
  17. Helanto M, Kiviharju K, Granström T, Leisola M, Nyyssölä A (2009) Biotechnological production of L-ribose from L-arabinose. Appl Microbiol Biotechnol 83(1):77–83.  https://doi.org/10.1007/s00253-008-1855-x CrossRefPubMedGoogle Scholar
  18. Hu X, Shi Y, Zhang P, Miao M, Zhang T, Jiang B (2016) D-mannose: properties, production, and applications: an overview. Compr Rev Food Sci F 15(4):773–785.  https://doi.org/10.1111/1541-4337.12211 CrossRefGoogle Scholar
  19. Ishige T, Honda K, Shimizu S (2005) Whole organism biocatalysis. Curr Opin Chem Biol 9(2):174–180.  https://doi.org/10.1016/j.cbpa.2005.02.001 CrossRefPubMedGoogle Scholar
  20. Izumori K (2006) Izumoring: a strategy for bioproduction of all hexoses. J Biotechnol 124(4):717–722.  https://doi.org/10.1016/j.jbiotec.2006.04.016 CrossRefPubMedGoogle Scholar
  21. Johnston K, Clements A, Venkataramani RN, Trievel RC, Marmorstein R (2000) Coexpression of proteins in bacteria using T7-based expression plasmids: expression of heteromeric cell-cycle and transcriptional regulatory complexes. Protein Expr Purif 20(3):435–443.  https://doi.org/10.1006/prep.2000.1313 CrossRefPubMedGoogle Scholar
  22. Kim KR, Seo ES, Oh DK (2014) L-ribose production from L-arabinose by immobilized recombinant Eescherichia coli co-expressing the L-arabinose isomerase and mannose-6-phosphate isomerase genes from Geobacillus thermodenitrificans. Appl Biochem Biotechnol 172(1):275–288.  https://doi.org/10.1007/s12010-013-0547-x CrossRefPubMedGoogle Scholar
  23. Kim NH, Kim HJ, Kang DI, Jeong KW, Lee JK, Kim Y, Oh DK (2008) Conversion shift of D-fructose to D-psicose for enzyme-catalyzed epimerization by addition of borate. Appl Environ Microbiol 74(10):3008–3013.  https://doi.org/10.1128/AEM.00249-08 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Korneeva OS, Cheremushkina IV, Glushchenko AS, Mikhaĭlova NA, Baturo AP, Romanenko ÉE, Zlygostev SA (2012) Prebiotic properties of mannose and its effect on specific resistance. Zhurnal Mikrobiol Epidemiol Immunobiol 5:67–70Google Scholar
  25. Kumar S, Tsai CJ, Nussinov R (2000) Factors enhancing protein thermostability. Protein Eng 13(3):179–191.  https://doi.org/10.1093/protein/13.3.179 CrossRefPubMedGoogle Scholar
  26. Kwon HJ, Yeom SJ, Park CS, Oh DK (2010) Substrate specificity of a recombinant D-lyxose isomerase from Providencia stuartii for monosaccharides. J Biosci Bioeng 110(1):26–31.  https://doi.org/10.1016/j.jbiosc.2009.12.011 CrossRefPubMedGoogle Scholar
  27. Lee SJ, Sang JL, Lee YJ, Kim SB, Kim SK, Lee DW (2012) Homologous alkalophilic and acidophilic L-arabinose isomerases reveal region-specific contributions to the pH dependence of activity and stability. Appl Environ Microbiol 78(24):8813–8816.  https://doi.org/10.1128/AEM.02114-12 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Lim BC, Kim HJ, Oh DK (2007) High production of D-tagatose by the addition of boric acid. Biotechnol Prog 23(4):824–828.  https://doi.org/10.1002/bp070056y CrossRefPubMedGoogle Scholar
  29. Long NVD, Le TH, Jinil K, Juweon L, Yoonmo K (2009) Separation of D-psicose and D-fructose using simulated moving bed chromatography. J Sep Sci 32(11):1987–1995.  https://doi.org/10.1002/jssc.200800753 CrossRefGoogle Scholar
  30. Marles-Wright J, Lewis RJ (2011) The structure of a D-lyxose isomerase from the σB regulon of Bacillus subtilis. Proteins 79(6):2015–2019.  https://doi.org/10.1002/prot.23028 CrossRefPubMedGoogle Scholar
  31. Mishra DK, Hwang JS (2013) Selective hydrogenation of D-mannose to D-mannitol using NiO-modified TiO 2 (NiO-TiO 2 ) supported ruthenium catalyst. Appl Catal A Gen 453(6):13–19.  https://doi.org/10.1016/j.apcata.2012.11.042 CrossRefGoogle Scholar
  32. Morita M, E S, K Y, Sakai T, Natori T, Koezuka Y, H F, K A (1996) Practical total synthesis of (2S,3S,4R)-1-O-(α-D-galactopyranosyl)-N-hexacosanoyl-2-amino-1,3,4-octadecanetriol, the antitumorial and immunostimulatory α-galactosylcer-amide, KRN7000. Biosci Biotechnol Biochem 60(2):288–292.  https://doi.org/10.1271/bbb.60.288 CrossRefPubMedGoogle Scholar
  33. Mozhaev VV (1993) Mechanism-based strategies for protein thermostabilization. Trends Biotechnol 11(3):88–95.  https://doi.org/10.1016/0167-7799(93)90057-G CrossRefPubMedGoogle Scholar
  34. Okano K (2009) Synthesis and pharmaceutical application of L-ribose. Tetrahedron 65(10):1937–1949.  https://doi.org/10.1016/j.tet.2008.11.047 CrossRefGoogle Scholar
  35. Park CS, Kwon HJ, Yeom SJ, Oh DK (2010a) Mannose production from fructose by free and immobilized D-lyxose isomerases from Providencia stuartii. Biotechnol Lett 32(9):1305–1309.  https://doi.org/10.1007/s10529-010-0300-2 CrossRefPubMedGoogle Scholar
  36. Park CS, Kim JE, Choi JG, Oh DK (2011) Characterization of a recombinant cellobiose 2-epimerase from Caldicellulosiruptor saccharolyticus and its application in the production of mannose from glucose. Appl Microbiol Biotechnol 92(6):1187–1196.  https://doi.org/10.1007/s00253-011-3403-3 CrossRefPubMedGoogle Scholar
  37. Park CS, Yeom SJ, Lim YR, Kim YS, Oh DK (2010b) Substrate specificity of a recombinant D-lyxose isomerase from Serratia proteamaculans that produces D-lyxose and D-mannose. Lett in. Appl Microbiol 51(3):343–350.  https://doi.org/10.1111/j.1472-765X.2010.02903.x CrossRefGoogle Scholar
  38. Patel DH, Wi SG, Lee SG, Lee DS, Song YH, Bae HJ (2011) Substrate specificity of the Bacillus licheniformis lyxose isomerase YdaE and its application in in vitro catalysis for bioproduction of lyxose and glucose by two-step isomerization. Appl Environ Microbiol 77(10):3343–3350.  https://doi.org/10.1128/AEM.02693-10 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Patel MJ, Akhani RC, Patel AT, Dedania SR, Patel DH (2017) A single and two step isomerization process for D-tagatose and L-ribose bioproduction using L-arabinose isomerase and D-lyxose isomerase. Enzym Microb Technol 97:27–33.  https://doi.org/10.1016/j.enzmictec.2016.11.001 CrossRefGoogle Scholar
  40. Shen SC, Wu JSB (2010) Maillard browning in ethanolic solution. J Food Sci 69(4):FCT273–FCT279Google Scholar
  41. Swenson CA, Barker R (1971) Proportion of keto and aldehydo forms in solutions of sugars and sugar phosphates. Biochemistry 10(16):3151–3154.  https://doi.org/10.1021/bi00792a026 CrossRefPubMedGoogle Scholar
  42. Van LS, Park CS, Yeom SJ, Adamscioaba MA, Oh DK, Jia Z (2010) Structure-based annotation of a novel sugar isomerase from the pathogenic E. coli O157:H7. J Mol Biol 401(5):866–881CrossRefGoogle Scholar
  43. Vuksan V, Jenkins DJ, Spadafora P, Sievenpiper JL, Owen R, Vidgen E, Brighenti F, Josse R, Leiter LA, Bruce-Thompson C (1999) Konjac-mannan (glucomannan) improves glycemia and other associated risk factors for coronary heart disease in type 2 diabetes. A randomized controlled metabolic trial. Diabetes Care 22(6):913–919.  https://doi.org/10.2337/diacare.22.6.913 CrossRefPubMedGoogle Scholar
  44. Wagner N, Bosshart A, Failmezger J, Bechtold M, Panke S (2015) A separation-integrated cascade reaction to overcome thermodynamic limitations in rare-sugar synthesis. Angew Chem Int Edit 54(14):4182–4186.  https://doi.org/10.1002/anie.201411279 CrossRefGoogle Scholar
  45. Xu W, Zhang W, Zhang T, Jiang B, Mu W (2016a) L-rhamnose isomerase and its use for biotechnological production of rare sugars. Appl Microbiol Biotechnol 100(7):1–8CrossRefGoogle Scholar
  46. Xu Z, Li S, Feng X, Liang J, Xu H (2014) L-arabinose isomerase and its use for biotechnological production of rare sugars. Appl Microbiol Biotechnol 98(21):8869–8878.  https://doi.org/10.1007/s00253-014-6073-0 CrossRefPubMedGoogle Scholar
  47. Xu Z, Sha Y, Liu C, Li S, Liang J, Zhou J, Xu H (2016b) L-ribose isomerase and mannose-6-phosphate isomerase: properties and applications for l-ribose production. Appl Microbiol Biotechnol 100(21):9003–9011.  https://doi.org/10.1007/s00253-016-7834-8 CrossRefPubMedGoogle Scholar
  48. Takagi Y, Nakai K, Tsuchiya T, Takeuchi T (1996) A 5′-(Trifluoromethyl)anthracycline glycoside: synthesis of antitumor-active 7-O-(2,6-Dideoxy-6,6,6-trifluoro-α-l-lyxo-hexopyranosyl)adriamycinone. J Med Chem 39(8):1582–1588CrossRefPubMedGoogle Scholar
  49. Yeom SJ, Ji JH, Kim NH, Park CS, Oh DK (2009) Substrate specificity of a mannose-6-phosphate isomerase from Bacillus subtilis and its application in the production of L-ribose. Appl Environ Microbiol 75(14):4705–4710.  https://doi.org/10.1128/AEM.00310-09 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Yu L, Zhang W, Zhang T, Jiang B, Mu W (2016) Efficient biotransformation of D-fructose to D-mannose by a thermostable D-lyxose isomerase from Thermosediminibacter oceani. Process Biochem 51(12):2026–2033.  https://doi.org/10.1016/j.procbio.2016.08.023 CrossRefGoogle Scholar
  51. Zhang D, Chia C, Jiao X, Jin W, Kasagi S, Wu R, Konkel JE, Nakatsukasa H, Zanvit P, Goldberg N, Chen Q, Sun L, Chen ZJ, Chen W (2017a) D-mannose induces regulatory T cells and suppresses immunopathology. Nat Med 23(9):1036–1045.  https://doi.org/10.1038/nm.4375 CrossRefPubMedGoogle Scholar
  52. Zhang W, Fang D, Xing Q, Zhou L, Jiang B, Mu W (2013) Characterization of a novel metal-dependent D-psicose 3-epimerase from Clostridium scindens 35704. PLoS One 8(4):e62987.  https://doi.org/10.1371/journal.pone.0062987 CrossRefPubMedPubMedCentralGoogle Scholar
  53. Zhang W, Li H, Zhang T, Jiang B, Zhou L, Mu W (2015) Characterization of a D-psicose 3-epimerase from Dorea sp. CAG317 with an acidic pH optimum and a high specific activity. J Mol Catal B Enzym 120:68–74.  https://doi.org/10.1016/j.molcatb.2015.05.018 CrossRefGoogle Scholar
  54. Zhang W, Yu S, Zhang T, Jiang B, Mu W (2016) Recent advances in D-allulose: physiological functionalities, applications, and biological production. Trends Food Sci Technol 54:127–137.  https://doi.org/10.1016/j.tifs.2016.06.004 CrossRefGoogle Scholar
  55. Zhang W, Zhang T, Jiang B, Mu W (2017b) Enzymatic approaches to rare sugar production. Biotechnol Adv 35(2):267–274.  https://doi.org/10.1016/j.biotechadv.2017.01.004 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jiawei Huang
    • 1
  • Ziwei Chen
    • 1
  • Wenli Zhang
    • 1
  • Tao Zhang
    • 1
    • 2
  • Wanmeng Mu
    • 1
    • 2
  1. 1.State Key Laboratory of Food Science and TechnologyJiangnan UniversityWuxiChina
  2. 2.Synergetic Innovation Center of Food Safety and NutritionJiangnan UniversityWuxiChina

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