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Efficient Allitol Bioproduction from d-Fructose Catalyzed by Recombinant E. coli Whole Cells, and the Condition Optimization, Product Purification

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Abstract

Allitol is a kind of rare sugar alcohol with potential application value. An engineered strain, which simultaneously expressed d-psicose-3-epimerase (DPE), ribitol dehydrogenase (RDH), and formate dehydrogenase (FDH) three enzymes, was constructed by cloning above three genes into one plasmid and transformed into the host E. coli strain, and used as the whole-cell catalysts for biotransformation of allitol from the low-cost substrate of d-fructose. The whole cell allitol biotransformation conditions were optimized. The medium, recombinant gene induction conditions, and the substrate feeding rate for cultivation of the catalytic cells were optimized. Then, the fed-batch culture was made and scaled up to 10 L fermentor. Finally, 63.44 g/L allitol was obtained from 100 g/L d-fructose after 3 h of biotransformation, and the allitol crystals of 99.9% purity were obtained by using cooling recrystallization. The allitol production method developed in this research has high product purity, and is highly efficient, easily scaled up, and suitable for large-scale production of highly purified allitol.

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References

  1. Takeshita, K., Ishida, Y., Takata, G., & Izumori, K. (2000). Direct production of allitol from D-fructose by a coupling reaction using D-tagatose-3-epimerase, ribitol dehydrogenase and formate dehydrogenase. Journal of Bioscience and Bioengineering, 90(5), 545–548. https://doi.org/10.1016/S1389-1723(01)80038-4.

    Article  PubMed  CAS  Google Scholar 

  2. Oosaka, K. (2009). Possible as monosaccharide laxative of rare sugar alcohols. Yakugaku Zasshi, 129(5), 575–580.

    Article  CAS  Google Scholar 

  3. Zhu, Y., Li, H., Liu, P., Yang, J., Zhang, X., & Sun, Y. (2015). Construction of allitol synthesis pathway by multi-enzyme coexpression in Escherichia coli and its application in allitol production. Journal of Industrial Microbiology and Biotechnology, 42(5), 661–669. https://doi.org/10.1007/s10295-014-1578-1.

    Article  PubMed  CAS  Google Scholar 

  4. Hassanin, H. A. M., Mu, W., Koko, M. Y. F., Zhang, T., Masamba, K., & Jiang, B. (2017). Allitol: production, properties and applications. International Journal of Food Science & Technology, 52(1), 91–97. https://doi.org/10.1111/ijfs.13290.

    Article  CAS  Google Scholar 

  5. Izumori, K. (2002). Bioproduction strategies for rare hexose sugars. Naturwissenschaften, 89(3), 120–124. https://doi.org/10.1007/s00114-002-0297-z.

    Article  PubMed  CAS  Google Scholar 

  6. Granström, T. B., Takata, G., Tokuda, M., & Izumori, K. (2004). Izumoring: a novel and complete strategy for bioproduction of rare sugars. Journal of Bioscience and Bioengineering, 97(2), 89–94. https://doi.org/10.1016/s1389-1723(04)70173-5.

    Article  PubMed  Google Scholar 

  7. Izumori, K. (2006). Izumoring: a strategy for bioproduction of all hexoses. Journal of Biotechnology, 124(4), 717–722. https://doi.org/10.1016/j.jbiotec.2006.04.016.

    Article  PubMed  CAS  Google Scholar 

  8. Wu, S. H., Luo, X. D., Ma, Y. B., Liu, J. K., Wu, D. G., Zhao, B., Lu, Y., & Zheng, Q. T. (2000). Two novel secoergosterols from the fungus Tylopilus plumbeoviolaceus. Journal of Natural Products, 63(4), 534–536. https://doi.org/10.1021/np990494h.

    Article  PubMed  CAS  Google Scholar 

  9. Zeng, Y., Dou, D., Zhang, Y., Zhang, L., & Sun, Y. (2014). Rare sugars and antioxidants in Itea virginica, Itea oblonga Hand.-Mazz.,and Itea yunnanensis Franch Leaves. International Journal of Food Properties, 18(11), 2549–2560. https://doi.org/10.1080/10942912.2014.917099.

    Article  CAS  Google Scholar 

  10. Jumde, V. R., Eisink, N. N., Witte, M. D., & Minnaard, A. J. (2016). C3 epimerization of glucose, via regioselective oxidation and reduction. The Journal of Organic Chemistry, 81(22), 11439–11443. https://doi.org/10.1021/acs.joc.6b02074.

    Article  PubMed  CAS  Google Scholar 

  11. Kim, H. J., Hyun, E. K., Kim, Y. S., Lee, Y. J., & Oh, D. K. (2006). Characterization of an Agrobacterium tumefaciens d-psicose 3-epimerase that converts d-fructose to d-psicose. Applied and Environmental Microbiology, 72(2), 981–985. https://doi.org/10.1128/AEM.72.2.981-985.2006.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  12. Hassanin, H. A., Wang, X., Mu, W., Zhang, T., & Jiang, B. (2016). Cloning and characterization of a new ribitol dehydrogenase from Providencia alcalifaciens RIMD 1656011. Journal of the Science of Food and Agriculture, 96(8), 2917–2924. https://doi.org/10.1002/jsfa.7589.

    Article  PubMed  CAS  Google Scholar 

  13. Hassanin, H. A. M., Letsididi, R., Koko, M. Y. F., Mu, W., Elferga, A., & Jiang, B. (2016). Synthesis of allitol from D-psicose using ribitol dehydrogenase and formate dehydrogenase. Tropical Journal of Pharmaceutical Research, 15(12), 2701–2708. https://doi.org/10.4314/tjpr.v15i12.23.

    Article  CAS  Google Scholar 

  14. He, X., Zhou, X., Yang, Z., Xu, L., Yu, Y., Jia, L., & Li, G. (2015). Cloning, expression and purification of d-tagatose 3-epimerase gene from Escherichia coli JM109. Protein Expression and Purification, 114, 77–81. https://doi.org/10.1016/j.pep.2015.06.015.

    Article  PubMed  CAS  Google Scholar 

  15. Muniruzzaman, S., Tokunaga, H., & Izumori, K. (1995). Conversion of d-psicose to allitol by Enterobacter agglomerans strain 221e. Journal of Fermentation and Bioengineering, 79(4), 323–327. https://doi.org/10.1016/0922-338X(95)93989-W.

    Article  CAS  Google Scholar 

  16. Han, W., Zhu, Y., Men, Y., Yang, J., Liu, C., & Sun, Y. (2014). Production of allitol from D-psicose by a novel isolated strain of Klebsiella oxytoca G4A4. Journal of Basic Microbiology, 54(10), 1073–1079. https://doi.org/10.1002/jobm.201300647.

    Article  PubMed  CAS  Google Scholar 

  17. Hassanin, H. A., Eassa, M. A., & Jiang, B. (2018). Facile synthesis of bioactive allitol from D-psicose by coexpression of ribitol dehydrogenase and formate dehydrogenase in Escherichia coli. Journal of Food Bioactives, 4, 117–122. https://doi.org/10.31665/JFB.20xx.000xx.

    Article  Google Scholar 

  18. Lu, F., Xu, W., Zhang, W., Guang, C., & Mu, W. (2019). Polyol dehydrogenases: intermediate role in the bioconversion of rare sugars and alcohols. Applied Microbiology and Biotechnology, 103(16), 6473–6481. https://doi.org/10.1007/s00253-019-09980-z.

    Article  PubMed  CAS  Google Scholar 

  19. Takeshita, K., Suga, A., Takada, G., & Izumori, K. (2000). Mass production of D-psicose from D-fructose by a continuous bioreactor system using immobilized D-tagatose 3-epimerase. Journal of Bioscience and Bioengineering, 90(4), 453–455. https://doi.org/10.1016/s1389-1723(01)80018-9.

    Article  PubMed  CAS  Google Scholar 

  20. Choi, J. G., Ju, Y. H., Yeom, S. J., & Oh, D. K. (2011). Improvement in the thermostability of D-psicose 3-epimerase from Agrobacterium tumefaciens by random and site-directed mutagenesis. Applied and Environmental Microbiology, 77(20), 7316–7320. https://doi.org/10.1128/AEM.05566-11.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Li, C., Lin, J., Guo, Q., Zhang, C., Du, K., Lin, H., & Lin, J. (2018). D-psicose 3-epimerase secretory overexpression, immobilization, and d-psicose biotransformation, separation and crystallization. Journal of Chemical Technology and Biotechnology, 93(2), 350–357. https://doi.org/10.1002/jctb.5360.

    Article  CAS  Google Scholar 

  22. Li, C., Zhang, C., Lin, J., Gao, L., Lin, H., & Lin, J. (2018). Enzymatic fructose removal from D-psicose bioproduction model solution and the system modeling and simulation. Journal of Chemical Technology and Biotechnology, 93(5), 1249–1260. https://doi.org/10.1002/jctb.5483.

    Article  CAS  Google Scholar 

  23. Makower, B., & Dye, W. B. (1956). Sugar crystallization, equilibrium moisture content and crystallization of amorphous sucrose and glucose. Journal of Agricultural and Food Chemistry, 4(1), 72–77. https://doi.org/10.1021/jf60059a010.

    Article  CAS  Google Scholar 

  24. Restaino, O. F., Bhaskar, U., Paul, P., Li, L., De Rosa, M., Dordick, J. S., & Linhardt, R. J. (2013). High cell density cultivation of a recombinant E. coli strain expressing a key enzyme in bioengineered heparin production. Applied Microbiology and Biotechnology, 97(9), 3893–3900. https://doi.org/10.1007/s00253-012-4682-z.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  25. Faust, G., Janzen, N. H., Bendig, C., Romer, L., Kaufmann, K., & Weuster-Botz, D. (2014). Feeding strategies enhance high cell density cultivation and protein expression in milliliter scale bioreactors. Biotechnology Journal, 9(10), 1293–1303. https://doi.org/10.1002/biot.201400346.

    Article  PubMed  CAS  Google Scholar 

  26. Chen, Y., Li, L., Long, L., & Ding, S. (2018). High cell-density cultivation of phenolic acid decarboxylase-expressing Escherichia coli and 4-vinylguaiacol bioproduction from ferulic acid by whole-cell catalysis. Journal of Chemical Technology and Biotechnology, 93(8), 2415–2421. https://doi.org/10.1002/jctb.5590.

    Article  CAS  Google Scholar 

  27. Priebe, X., Daschner, M., Schwab, W., & Weuster-Botz, D. (2018). Rational selection of biphasic reaction systems for geranyl glucoside production by Escherichia coli whole-cell biocatalysts. Enzyme and Microbial Technology, 112, 79–87. https://doi.org/10.1016/j.enzmictec.2017.11.003.

    Article  PubMed  CAS  Google Scholar 

  28. Zhu, Y., Men, Y., Bai, W., Li, X., Zhang, L., Sun, Y., & Ma, Y. (2012). Overexpression of d-psicose 3-epimerase from Ruminococcus sp. in Escherichia coli and its potential application in d-psicose production. Biotechnology Letters, 34(10), 1901–1906. https://doi.org/10.1007/s10529-012-0986-4.

    Article  PubMed  Google Scholar 

  29. 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.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  30. Ferenci, T., & Kornberg, H. L. (1973). The utilization of fructose by Escherichia coli. Properties of a mutant defective in fructose-1-phosphate kinase activety. Biochemical Journal, 132(2), 341–347. https://doi.org/10.1042/bj1320341.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  31. Ferenci, T., & Kornberg Hans, L. (1974). The role of phosphotransferase-mediated syntheses of fructose 1-phosphate and fructose 6-phosphate in the growth of Escherichia coli on fructose. Proceedings of the Royal Society B: Biological Sciences, 187(1087), 105–119. https://doi.org/10.1098/rspb.1974.0065.

    Article  CAS  Google Scholar 

  32. Kornberg, H. L., Lambourne, L. T. M., & Sproul, A. A. (2000). Facilitated diffusion of fructose via the phosphoenolpyruvate/glucose phosphotransferase system of Escherichia coli. Proceedings of the National Academy of Sciences, 97(4), 1808–1812. https://doi.org/10.1073/pnas.97.4.1808.

    Article  CAS  Google Scholar 

  33. Pastor, J. M., Borges, N., Pagan, J. P., Castano-Cerezo, S., Csonka, L. N., Goodner, B. W., Reynolds, K. A., Goncalves, L. G., Argandona, M., Nieto, J. J., Vargas, C., Bernal, V., & Canovas, M. (2019). Fructose metabolism in Chromohalobacter salexigens: interplay between the embden-meyerhof-parnas and entner-doudoroff pathways. Microbial Cell Factories, 18(1), 134–148. https://doi.org/10.1186/s12934-019-1178-x.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Ji, X. J., Huang, H., Du, J., Zhu, J. G., Ren, L. J., Li, S., & Nie, Z. K. (2009). Development of an industrial medium for economical 2,3-butanediol production through co-fermentation of glucose and xylose by Klebsiella oxytoca. Bioresource Technology, 100(21), 5214–5218. https://doi.org/10.1016/j.biortech.2009.05.036.

    Article  PubMed  CAS  Google Scholar 

  35. Ye, Q., Li, X., Yan, M., Cao, H., Xu, L., Zhang, Y., Chen, Y., Xiong, J., Ouyang, P., & Ying, H. (2010). High-level production of heterologous proteins using untreated cane molasses and corn steep liquor in Escherichia coli medium. Applied Microbiology and Biotechnology, 87(2), 517–525. https://doi.org/10.1007/s00253-010-2536-0.

    Article  PubMed  CAS  Google Scholar 

  36. Borji, A., & Jourani, A. (2018). Spectrophotometry as a method for the determination of solubility of sucrose in water and metastable zone width of its aqueous solutions. Crystal Research and Technology, 53(6), 1700123–1700128. https://doi.org/10.1002/crat.201700123.

    Article  CAS  Google Scholar 

  37. Shao, X. F., Yang, S., Wang, C., Yang, Y. J., Wang, W. J., Zeng, Y., & Fan, L. W. (2019). Screening of sugar alcohols and their binary eutectic mixtures as phase change materials for low-to-medium temperature thermal energy storage. (II): Isothermal melting and crystallization behaviors. Energy, 180, 572–583. https://doi.org/10.1016/j.energy.2019.05.109.

    Article  CAS  Google Scholar 

  38. Singh, K., Gupta, S. P., Kumar, A., & Kumar, A. (2019). The effect of high intensity ultrasound (HIU) on the kinetics of crystallization of sucrose: elimination of latent period. Ultrasonics-Sonochemistry, 52, 19–24. https://doi.org/10.1016/j.ultsonch.2018.05.030.

    Article  PubMed  CAS  Google Scholar 

  39. Kaup, B., Bringer-Meyer, S., & Sahm, H. (2004). Metabolic engineering of Escherichia coli: construction of an efficient biocatalyst for d-mannitol formation in a whole-cell biotransformation. Applied Microbiology and Biotechnology, 64(3), 333–339. https://doi.org/10.1007/s00253-003-1470-9.

    Article  PubMed  CAS  Google Scholar 

  40. Lin, J. Q., Lee, S. M., & Koo, Y. M. (2001). Hydrolysis of paper mill sludge using an improved enzyme system. Journal of Microbiology and Biotechnology, 11(3), 362–368.

    CAS  Google Scholar 

  41. Alekseeva, A. A., Fedorchuk, V. V., Zarubina, S. A., Sadykhov, E. G., Matorin, A. D., Savin, S. S., & Tishkov, V. I. (2015). The role of Ala198 in the stability and coenzyme specificity of bacterial formate dehydrogenases. Acta Naturae, 7(1), 60–69.

    Article  CAS  Google Scholar 

  42. Li, C., Lin, J. Q., Gao, L., Lin, H. B., & Lin, J. Q. (2018). Modeling and simulation of enzymatic gluconic acid production using immobilized enzyme and CSTR–PFTR circulation reaction system. Biotechnology Letters, 40(4), 649–657. https://doi.org/10.1007/s10529-018-2509-4.

    Article  PubMed  CAS  Google Scholar 

  43. Huang, R., Chen, H., Zhong, C., Kim, J. E., & Zhang, Y. H. (2016). High-throughput screening of coenzyme preference change of thermophilic 6-phosphogluconate dehydrogenase from NADP+ to NAD+. Scientific Reports, 6, 32644–32644. https://doi.org/10.1038/srep32644.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

The authors would like to thank Chengjia Zhang, Caiyun Sun from the Core Facilities for Life and Environmental Sciences, State Key Lab of Microbial Technology for help and guidance in the experiments.

Funding

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

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Correspondence to Xin Song or Jianqiang Lin.

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Wen, X., Lin, H., Ren, Y. et al. Efficient Allitol Bioproduction from d-Fructose Catalyzed by Recombinant E. coli Whole Cells, and the Condition Optimization, Product Purification. Appl Biochem Biotechnol 192, 680–697 (2020). https://doi.org/10.1007/s12010-020-03359-x

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