Skip to main content
SpringerLink
Log in

Bioconversion of d-glucose to d-psicose with immobilized d-xylose isomerase and d-psicose 3-epimerase on Saccharomyces cerevisiae spores

  • Biotechnology Methods
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

Saccharomyces cerevisiae spores are dormant cells, which can tolerate various types of environmental stress. In our previous work, we successfully developed biological and chemical methods for enzyme immobilization based on the structures of S. cerevisiae spore wall. In this study, we employed biological and chemical approaches for the immobilization of d-xylose isomerase (XI) from Thermus thermophilus and d-psicose 3-epimerase (DPEase) from Agrobacterium tumefaciens with yeast spores, respectively. The enzymatic properties of both immobilized XI and DPEase were characterized and the immobilized enzymes exhibit higher thermostability, broader pH tolerance, and good repeatability compared with free enzymes. Furthermore, we established a two-step approach for the bioconversion of d-glucose to d-psicose using immobilized enzymes. To improve the conversion yield, a multi-pot strategy was adopted for d-psicose production by repeating the two-step process continually. As a result, the yield of d-psicose was obviously improved and the highest yield reached about 12.0 %.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Scheme 1
Fig. 5

Similar content being viewed by others

References

  1. Biro E, Nemeth AS, Sisak C, Feczko T, Gyenis J (2008) Preparation of chitosan particles suitable for enzyme immobilization. J Biochem Biophys Methods 70:1240–1246

    Article  CAS  PubMed  Google Scholar 

  2. Botts MR, Giles SS, Gates MA, Kozel TR, Hull CM (2009) Isolation and characterization of Cryptococcus neoformans spores reveal a critical role for capsule biosynthesis genes in spore biogenesis. Eukaryot Cell 8:595–605

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Brat D, Boles E, Wiedemann B (2009) Functional expression of a bacterial xylose isomerase in Saccharomyces cerevisiae. Appl Environ Microbiol 75:2304–2311

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  4. Briza P, Breitenbach M, Ellinger A, Segall J (1990) Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev 4:1775–1789

    Article  CAS  PubMed  Google Scholar 

  5. Briza P, Ellinger A, Winkler G, Breitenbach M (1990) Characterization of a DL-dityrosine-containing macromolecule from yeast ascospore walls. J Biol Chem 265:15118–15123

    CAS  PubMed  Google Scholar 

  6. Briza P, Kalchhauser H, Pittenauer E, Allmaier G, Breitenbach M (1996) N,N′-Bisformyl dityrosine is an in vivo precursor of the yeast ascospore wall. Eur J Biochem 239:124–131

    Article  CAS  PubMed  Google Scholar 

  7. Briza P, Winkler G, Kalchhauser H, Breitenbach M (1986) Dityrosine is a prominent component of the yeast ascospore wall. A proof of its structure. J Biol Chem 261:4288–4294

    CAS  PubMed  Google Scholar 

  8. Choi JG, Ju YH, Yeom SJ, Oh DK (2011) Improvement in the thermostability of d-psicose 3-epimerase from Agrobacterium tumefaciens by random and site-directed mutagenesis. Appl Environ Microbiol 77:7316–7320

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Itoh H, Okaya H, Khan A, Tajima S, Hayakawa S, Izumori K (1994) Purification and characterization of d-tagatose 3-epimerase from Pseudomonas sp. ST-24. Biosci Biotechnol Biochem 58:2168–2171

    Article  CAS  Google Scholar 

  10. Itoh H, Sato T, Izumori K (1995) Preparation of d-psicose from d-fructose by immobilized d-tagatose 3-epimerase. J Ferment Bioeng 80:101–103

    Article  CAS  Google Scholar 

  11. Jia M, Mu W, Chu F, Zhang X, Jiang B, Zhou LL, Zhang T (2014) A d-psicose 3-epimerase with neutral pH optimum from Clostridium bolteae for d-psicose production: cloning, expression, purification, and characterization. Appl Microbiol Biotechnol 98:717–725

    Article  CAS  PubMed  Google Scholar 

  12. Kim HJ, Hyun EK, Kim YS, Lee YJ, Oh DK (2006) Characterization of an Agrobacterium tumefaciens d-psicose 3-epimerase that converts d-fructose to d-psicose. Appl Environ Microbiol 72:981–985

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  13. Kloimwieder A, Winston F (2011) A screen for germination mutants in Saccharomyces cerevisiae. G3-Genes Genom Genet 1:143–149

    CAS  Google Scholar 

  14. Kupiec M, Byers B, Esposito RE, Mitchell AP (1997) The molecular and cell biology of the yeast Saccharomyces. In: Pringle JR, Jones EW (eds) Meiosis and Sporulation in Saccharomyces cerevisiae. Cold Spring Harbor Laboratory Press, New York, pp 889–1036

    Google Scholar 

  15. Kuyper M, Harhangi HR, Stave AK, Winkler AA, Jetten MS, Laat WT, Ridder JJ, Op den Camp HJ, Dijken JP, Pronk JT (2003) High-level functional expression of a fungal xylose isomerase: the key to efficient ethanolic fermentation of xylose by Saccharomyces cerevisiae? FEMS Yeast Res 4:69–78

    Article  CAS  PubMed  Google Scholar 

  16. Lin CP, Kim C, Smith SO, Neiman AM (2013) A highly redundant gene network controls assembly of the outer spore wall in S. cerevisiae. PLoS Genet 9:e1003700

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  17. Madhavan A, Tamalampudi S, Ushida K, Kanai D, Katahira S, Srivastava A, Fukuda H, Bisaria VS, Kondo A (2009) Xylose isomerase from polycentric fungus Orpinomyces: gene sequencing, cloning, and expression in Saccharomyces cerevisiae for bioconversion of xylose to ethanol. Appl Microbiol Biotechnol 82:1067–1078

    Article  CAS  PubMed  Google Scholar 

  18. Matsuo T, Suzuki H, Hashiguchi M, Izumori K (2002) d-psicose is a rare sugar that provides no energy to growing rats. J Nutr Sci Vitaminol 48:77–80

    Article  CAS  PubMed  Google Scholar 

  19. Men Y, Zhu Y, Zeng Y, Izumori K, Sun Y, Ma Y (2014) Co-expression of d-glucose isomerase and d-psicose 3-epimerase: development of an efficient one-step production of d-psicose. Enzyme Microb Technol 64–65:1–5

    Article  PubMed  Google Scholar 

  20. Mu W, Chu F, Xing Q, Yu S, Zhou L, Jiang B (2011) Cloning, expression, and characterization of a d-psicose 3-epimerase from Clostridium cellulolyticum H10. J Agric Food Chem 59:7785–7792

    Article  CAS  PubMed  Google Scholar 

  21. Mu W, Zhang W, Fang D, Zhou L, Jiang B, Zhang T (2013) Characterization of a d-psicose-producing enzyme, d-psicose 3-epimerase, from Clostridium sp. Biotechnol Lett 35(9):1481–1486

    Article  CAS  PubMed  Google Scholar 

  22. Mumberg D, Müller R, Funk M (1995) Yeast vectors for the controlled expression of heterologous proteins in different genetic backgrounds. Gene 156:119–122

    Article  CAS  PubMed  Google Scholar 

  23. Neiman AM (2011) Sporulation in the budding yeast Saccharomyces cerevisiae. Genetics 189:737–765

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  24. Neiman AM, Katz L, Brennwald PJ (2000) Identification of domains required for developmentally regulated SNARE function in Saccharomyces cerevisiae. Genetics 155:1643–1655

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Ota M, Sakuragi H, Morisaka H, Kuroda K, Miyake H, Tamaru Y, Ueda M (2013) Display of Clostridium cellulovorans xylose isomerase on the cell surface of Saccharomyces cerevisiae and its direct application to xylose fermentation. Biotechnol Prog 29:346–351

    Article  CAS  PubMed  Google Scholar 

  26. Pammer M, Briza P, Ellinger A, Schuster T, Stucka R, Feldmann H, Breitenbach M (1992) DIT101 (CSD2, CAL1), a cell cycle-regulated yeast gene required for synthesis of chitin in cell walls and chitosan in spore walls. Yeast 8:1089–1099

    Article  CAS  PubMed  Google Scholar 

  27. Pospiskova K, Safarik I (2013) Low-cost, easy-to-prepare magnetic chitosan microparticles for enzymes immobilization. Carbohydr Polym 96:545–548

    Article  CAS  PubMed  Google Scholar 

  28. Shi L, Li Z, Tachikawa H, Gao X-D, Nakanishi H (2014) Use of yeast spores for microencapsulation of enzymes. Appl Environ Microbiol 80:4502–4510

    Article  PubMed Central  PubMed  Google Scholar 

  29. Suda Y, Rodriguez RK, Coluccio AE, Neiman AM (2009) A screen for spore wall permeability mutants identifies a secreted protease required for proper spore wall assembly. PLoS One 4:e7184

    Article  PubMed Central  PubMed  Google Scholar 

  30. Sun Y, Hayakawa S, Ogawa M, Fukada K, Izumori K (2008) Influence of a rare sugar, d-psicose, on the physicochemical and functional properties of an aerated food system containing egg albumen. J Agric Food Chem 56:4789–4796

    Article  CAS  PubMed  Google Scholar 

  31. Susanto H, Samsudin AM, Rokhati N, Widiasa IN (2013) Immobilization of glucose oxidase on chitosan-based porous composite membranes and their potential use in biosensors. Enzyme Microb Technol 52:386–392

    Article  CAS  PubMed  Google Scholar 

  32. 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. J Biosci Bioeng 90:453–455

    Article  CAS  PubMed  Google Scholar 

  33. Uechi K, Takata G, Fukai Y, Yoshihara A, Morimoto K (2013) Gene cloning and characterization of l-ribulose 3-epimerase from Mesorhizobium loti and its application to rare sugar production. Biosci Biotechnol Biochem 77(3):511–515

    Article  CAS  PubMed  Google Scholar 

  34. Walfridsson M, Bao X, Anderlund M, Lilius G, Bülow L, Hahn-Hägerdal B (1996) Ethanolic fermentation of xylose with Saccharomyces cerevisiae harboring the Thermus thermophilus xylA gene, which expresses an active xylose (glucose) isomerase. Appl Environ Microbiol 62:4648–4651

    CAS  PubMed Central  PubMed  Google Scholar 

  35. Zhang H, Tachikawa H, Gao X-D, Nakanishi H (2014) Applied uses of yeast spores as chitosan beads. Appl Environ Microbiol 80:5098–5105

    Article  PubMed Central  PubMed  Google Scholar 

  36. Zhang L, Mu W, Jiang B, Zhang T (2009) Characterization of d-tagatose-3-epimerase from Rhodobacter sphaeroides that converts d-fructose into d-psicose. Biotechnol Lett 31:857–862

    Article  CAS  PubMed  Google Scholar 

  37. 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:e62987

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  38. Zhang W, Fang D, Zhang T, Zhou L, Jiang B, Mu W (2013) Characterization of a metal-dependent d-psicose 3-epimerase from a novel strain, Desmospora sp. 8437. J Agric Food Chem 61(47):11468–11476

    Article  CAS  PubMed  Google Scholar 

  39. Zhang W, Zhang T, Jiang B, Mu W (2015) Biochemical characterization of a d-psicose 3-epimerase from Treponema primitia ZAS-1 and its application on enzymatic production of d-psicose. J Sci Food Agric. doi:10.1002/jsfa.7187

    Google Scholar 

  40. 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. Biotechnol Lett 34:1901–1906

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Natural Science Foundation of China (21302069), China Postdoctoral Science Foundation (2014M551500), the Key Project of Chinese Ministry of Education (313027), Fundamental Research Funds for the Central Universities (JUSRP1003), 111 Project (No. 111-2-06), and Agriculture Science Technology Achievement Transformation Fund (2014GB2A000268).

Conflict of interest

The authors declare that they have no conflict of interest.

Compliance with ethical standards

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

Author information

Author notes

    Authors and Affiliations

    1. Key Laboratory of Carbohydrate Chemistry and Biotechnology, Ministry of Education, School of Biotechnology, Jiangnan University, Wuxi, 214122, China

      Zijie Li, Yi Li, Hideki Nakanishi & Xiao-Dong Gao

    2. China National Research Institute of Food and Fermentation Industries, Beijing, 10015, China

      Shenglin Duan, Jia Liu & Peng Yuan

    Authors
    1. Zijie Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Yi Li
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Shenglin Duan
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Jia Liu
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Peng Yuan
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Hideki Nakanishi
      View author publications

      You can also search for this author in PubMed Google Scholar

    7. Xiao-Dong Gao
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding authors

    Correspondence to Hideki Nakanishi or Xiao-Dong Gao.

    Additional information

    Z. Li and Y. Li contributed equally to this work.

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Li, Z., Li, Y., Duan, S. et al. Bioconversion of d-glucose to d-psicose with immobilized d-xylose isomerase and d-psicose 3-epimerase on Saccharomyces cerevisiae spores. J Ind Microbiol Biotechnol 42, 1117–1128 (2015). https://doi.org/10.1007/s10295-015-1631-8

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s10295-015-1631-8

    Keywords

    Search

    Navigation