Skip to main content
Log in

Construction of recombinant Escherichia coli expressing xylitol-4-dehydrogenase and optimization for enhanced L-xylulose biotransformation from xylitol

  • Research Paper
  • Published:
Bioprocess and Biosystems Engineering Aims and scope Submit manuscript

Abstract

L-Xylulose is a rare ketopentose which inhibits α-glucosidase and is an indicator of hepatitis or liver cirrhosis. This pentose is also a precursor of other rare sugars such as L-xylose, L-ribose or L-lyxose. Recombinant E. coli expressing xylitol-4-dehydrogenase gene of Pantoea ananatis was constructed. A cost-effective culture media were used for L-xylulose production using the recombinant E. coli strain constructed. Response surface methodology was used to optimize these media components for L-xylulose production. A high conversion rate of 96.5% was achieved under an optimized pH and temperature using 20 g/L xylitol, which is the highest among the reports. The recombinant E. coli cells expressing the xdh gene were immobilized in calcium alginate to improve recycling of cells. Effective immobilization was achieved with 2% (w/v) sodium alginate and 3% (w/v) calcium chloride. The immobilized E. coli cells retained good stability and enzyme activity for 9 batches with conversion between 53 and 92% which would be beneficial for economical production of L-xylulose.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Zhang W, Zhang T, Jiang B, Mu W (2017) Enzymatic approaches to rare sugar production. BiotechnolAdv 35:267–274

    CAS  Google Scholar 

  2. Bilal M, Iqbal HMN, Hu H, Wang W, Zhang X (2018) Metabolic engineering pathways for rare sugars biosynthesis, physiological functionalities, and applications—a review. Crit Rev Food SciNutr 58:2768–2778

    Article  CAS  Google Scholar 

  3. Beerens K, Desmet T, Soetaert W (2012) Enzymes for the biocatalytic production of rare sugars. J IndMicrobiolBiotechnol 39:823–834

    CAS  Google Scholar 

  4. Meng Q, Zhang T, Jiang B, Mu W, Miao M (2016) Advances in applications, metabolism, and biotechnological production of L-xylulose. ApplMicrobiolBiotechnol 100:535–540

    CAS  Google Scholar 

  5. Muniruzzaman S, Pan YT, Zeng Y, Atkins B, Izumori K, Elbein AD (1996) Inhibition of glycoprotein processing by L-fructose and L-xylulose. Glycobiology 6:795–803

    Article  CAS  PubMed  Google Scholar 

  6. Fang Z, Zhang W, Zhang T, Guang C, Mu W (2018) Isomerases and epimerases for biotransformation of pentoses. ApplMicrobiolBiotechnol 102:7283–7292

    CAS  Google Scholar 

  7. Shabat D, List B, Lerner RA, Barbas CF (1999) A short enantioselective synthesis of l-deoxy-L-xylulose by antibody catalysis. Tetrahedron Lett 40:1437–1440

    Article  CAS  Google Scholar 

  8. Glatthaar C, Reichstein T (1935) D-Adonose (D-Erythro-2-keto-pentose). HelvChimActa 18:80–81

    CAS  Google Scholar 

  9. Larson HW, Blatherwick N, Bradshaw PJ, Ewing ME, Sawyer SD (1941) The metabolism of L-xylulose. J BiolChem 138:353–360

    CAS  Google Scholar 

  10. Kim SJ, Kim YS, Yeom SJ (2020) Phosphate sugar isomerases and their potential for rare sugar bioconversion. J Microbiol 58:725–733

    Article  CAS  PubMed  Google Scholar 

  11. Drueckhammer DG, Durrwachter JR, Pederson RL, Crans DC, Daniels L, Wong CH (1989) Reversible and in situ formation of organic arsenates and vanadates as organic phosphate mimics in enzymatic reactions: mechanistic investigation of aldol reactions and synthetic applications. J Org Chem 54:70–77

    Article  CAS  Google Scholar 

  12. Richard P, Londesborough J, Putkonen M, Kalkkinen N, Penttilä M (2001) Cloning and expression of a fungal L-arabinitol 4-dehydrogenase gene. J BiolChem 276:40631–40637

    CAS  Google Scholar 

  13. Suzuki T, Tran LH, Yogo M, Idota O, Kitamoto N, Kawai K, Takamizawa K (2005) Cloning and expression of NAD+-dependent L-arabinitol 4-dehydrogenase gene (ladA) of Aspergillus oryzae. J BiosciBioeng 100:472–474

    CAS  Google Scholar 

  14. Tiwari MK, Singh RK, Gao H, Kim T, Chang S, Kim HS, Lee JK (2014) pH-rate profiles of L-arabinitol 4-dehydrogenase from Hypocrea jecorina and its application in L-xylulose production. Bioorg Med ChemLett 24:173–176

    Article  CAS  Google Scholar 

  15. Gao H, Kim IW, Choi JH, Khera E, Wen F, Lee JK (2015) Repeated production of L-xylulose by an immobilized whole-cell biocatalyst harboring L-arabinitol dehydrogenase coupled with an NAD+ regeneration system. BiochemEng J 96:23–28

    CAS  Google Scholar 

  16. Lu F, Xu W, Zhang W (2019) Polyol dehydrogenases: intermediate role in the bioconversion of rare sugars and alcohols. ApplMicrobiolBiotechnol 103:6473–6481

    CAS  Google Scholar 

  17. Hollmann S, Touster O (1957) The L-xylulose-xylitol enzyme and other polyol dehydrogenases of guinea pig liver mitochondria. J BiolChem 225:87–102

    CAS  Google Scholar 

  18. Doten RC, Mortlock RP (1985) Production of D-and L-xylulose by mutants of Klebsiella pneumoniae and Erwinia uredovora. Appl Environ Microbiol 49:158–162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Khan AR, Tokunaga H, Yoshida K, Izumori K (1991) Conversion of xylitol to L-xylulose by Alcaligenes sp. 701B-cells. J Ferment Bioeng 72:488–490

    Article  CAS  Google Scholar 

  20. Granstrom TB, Takata G, Morimoto K, Leisola M, Izumori K (2005) L-xylose and L-lyxose production from xylitol using Alcaligenes 701B strain and immobilized L-rhamnoseisomerase enzyme. EnzymeMicrobTechnol 36:976–981

    Google Scholar 

  21. Poonperm W, Takata G, Morimoto K, Granström TB, Izumori K (2007) Production of L-xylulose from xylitol by a newly isolated strain of Bacillus pallidus Y25 and characterization of its relevant enzyme xylitol dehydrogenase. Enzyme Microb Tech 40:1206–1212

    Article  CAS  Google Scholar 

  22. Zhang Y, Zhao X, Yang L, Han Y, Liu J (2014) Isolation and identification of a novel L-xylulose-producing strain. Food Sci 35:99–203

    Google Scholar 

  23. Aarnikunnas J, Pihlajaniemi A, Palva A, Leisola M, Nyyssölä A (2006) Cloning and expression of a xylitol-4-dehydrogenase gene from Pantoea ananatis. Appl Environ Microb 72:368–377

    Article  CAS  Google Scholar 

  24. Usvalampi A, Kiviharju K, Leisola M, Nyyssölä A (2009) Factors affecting the production of L-xylulose by resting cells of recombinant Escherichia coli. J IndMicrobiolBiot 36:1323–2133

    CAS  Google Scholar 

  25. Han Qi, Eiteman MA (2017) Coupling xylitol dehydrogenase with NADH oxidase improves L-xylulose production in Escherichia coli culture. Enzyme Microb Tech 106:106–113

    Article  CAS  Google Scholar 

  26. Takata G, Poonperm W, Morimoto K, Izumori K (2010) Cloning and overexpression of the xylitol dehydrogenase gene from Bacillus pallidus and its application to L-xylulose production. Biosci Biotech Bioch 74:1807–1813

    Article  CAS  Google Scholar 

  27. Arsenis C, Touster O (1969) Nicotinamide adenine dinucleotide phosphate-linked xylitol dehydrogenase in guinea pig liver cytosol. J BiolChem 244:3895–3899

    CAS  Google Scholar 

  28. Ishikura S, Isaji T, Usami N., Kitahara K, Nakagawa J and Hara A (2001) Molecular cloning, expression and tissue distribution of hamster diacetyl reductase. Identity with L-xylulose reductase, Chemico-Biol Int 879–889

  29. Nakagawa J, Ishikura S, Asami J, Isaji T, Usami N, Hara A, Sakurai T, Tsuritani K, Oda K, Takahashi M, Yoshimoto M, Otsuka N, Kitamura K (2002) Molecular characterization of mammalian dicarbonyl/L-xylulose reductase and its localization in kidney. J BiolChem 277:17883–17891

    CAS  Google Scholar 

  30. Verho R, Putkonen M, Londesborough J, Penttilä M, Richard P (2004) A novel NADH-linked L-xylulose reductase in the L-arabinose catabolic pathway of yeast. J BiolChem 279:14746–14751

    CAS  Google Scholar 

  31. Ye Q, Li XM, Yan M, Cao H, Xu L, Zhang YY, Chen Y, Xiong J, Ouyang PK, Ying HJ (2010) High-level production of heterologous proteins using untreated cane molasses and corn steep liquor in Escherichia coli medium. ApplMicrobiolBiotechnol 87:517–525

    CAS  Google Scholar 

  32. Li S, Xu H, Yu J, Wang Y, Feng X, Ouyang P (2013) Enhancing isomaltulose production by recombinant Escherichia coli producing sucrose isomerase: culture medium optimization containing agricultural wastes and cell immobilization. Bioprocess BiosystEng 36:1395–1405

    Article  CAS  Google Scholar 

  33. Lunzer R, Mamnun Y, Haltrich D, Kulbe KD, Nidetzky B (1998) Structural and functional properties of a yeast xylitol dehydrogenase, a Zn2+-containing metalloenzyme similar to medium-chain sorbitol dehydrogenases. Biochem J 336:91–99

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Kim TS, Gao H, Li J, Kalia VC, Muthusamy K, Sohng JK, Kim IW, Lee JK (2019) Overcoming NADPH product inhibition improves D-sorbitol conversion to L-sorbose. Sci Rep 9:1–9

    Google Scholar 

  35. Cor FBW, Frans W, Ronald B, Jaap V (1994) Isolation and characterization of two xylitol dehydrogenases from Aspergillus niger. Microbiol 140:1679–1685

    Article  Google Scholar 

  36. Erian AM, Gibisch M, Pflügl S (2018) Engineered E. coli W enables efficient 2,3-butanediol production from glucose and sugar beet molasses using defined minimal medium as economic basis. Microb Cell Fact 17:1–17

    Article  Google Scholar 

  37. Mendonça EHM, Avanci NC, Romano LH, Branco DL, de Pádua AX, Ward RJ, Neto ÁdB, Lourenzoni MR (2020) Recombinant xylanase production by Escherichia coli using a non-induced expression system with different nutrient sources Braz. J ChemEng 37:29–39

    Google Scholar 

  38. Agarwal L, Isar J, Dutt K, Saxena RK (2007) Statistical optimization for succinic acid production from E. coli in a cost-effective medium. ApplBiochemBiotechnol 142:158–167

    CAS  Google Scholar 

  39. Agarwal L, Isar J, Meghwanshi GK, Saxena RK (2006) A cost effective fermentative production of succinic acid from cane molasses and corn steep liquor by Escherichia coli. J ApplMicrobiol 100:1348–1354

    CAS  Google Scholar 

  40. Jahreis K, Bentler L, Bockmann J, Hans S, Meyer A, Siepelmeyer J, Lengeler JW (2002) Adaptation of sucrose metabolism in the Escherichia coli wild-type strain EC3132. J Bacteriol 184:5307–5316

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lee PC, Lee SY, Hong SH, Chang HN, Park SC (2003) Biological conversion of wood hydrolysate to succinic acid by Anaerobiospirillum succiniciproducens. BiotechnolLett 25:111–114

    CAS  Google Scholar 

  42. Smrdel P, Bogataj M, Mrhar A (2008) The influence of selected parameters on the size and shape of alginate beads prepared by ionotropic Gelation. Sci Pharm 76(1):77–89

    Article  CAS  Google Scholar 

  43. Idris A, Wahidin S (2006) Effect of sodium alginate concentration, bead diameter, initial pH and temperature on lactic acid production from pineapple waste using immobilized Lactobacillus delbrueckii. Process Biochem 41:1117–1123

    Article  CAS  Google Scholar 

  44. Lee KY, Mooney DJ (2012) Alginate: properties and biomedical applications. ProgPolymSci 37:106–126

    CAS  Google Scholar 

  45. Chen XH, Wang XT et al (2012) Immobilization of Acetobacter sp. CCTCC M209061 for efficient asymmetric reduction of ketones and biocatalyst recycling. Microb Cell Fact 11:119–131

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This research was funded by the Key R & D Plan of Shandong Province in 2019 (2019GSF107015), Shandong Province Science and Technology Development Project of China (2015GSF121016) and National Key Research and Development project of China (2017YFC1701502,2017YFC1701504).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Jianqiang Lin or Jianqun Lin.

Ethics declarations

Conflict of interest

All the authors declare that there is no conflict of interest.

Ethical statement

The authors declare that there are no studies conducted with human participants or animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOC 63 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tesfay, M.A., Wen, X., Liu, Y. et al. Construction of recombinant Escherichia coli expressing xylitol-4-dehydrogenase and optimization for enhanced L-xylulose biotransformation from xylitol. Bioprocess Biosyst Eng 44, 1021–1032 (2021). https://doi.org/10.1007/s00449-020-02505-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00449-020-02505-3

Keywords

Navigation