Skip to main content
SpringerLink
Log in

Optimization of recombinant Zea mays transglutaminase production and its influence on the functional properties of yogurt

  • Published:
Food Science and Biotechnology Aims and scope Submit manuscript

Abstract

The requirements for the production of optimized Zea mays transglutaminase (TGZo) using Pichia pastoris GS115 (pPIC9K-tgzo) were optimized in this study. Plackett–Burman design was used to screen variables that significantly influence TGZo production. Oleic acid, methanol, and loading volume were identified as the most significant parameters. Central composite design was employed to determine the optimal level of these three parameters for TGZo production. Results showed that 1078 mU/mL of TGZo activity and 7.6 mg/L of TGZo production were obtained under conditions of 0.07% oleic acid, 1.31% methanol, and 7.36% loading volume. To explore the functional characteristics of TGZo, it was used in yogurt. It was found that the addition of TGZo could produce yogurt with stronger acid gel and higher consistency, cohesiveness, index of viscosity, and apparent viscosity than the untreated product. Therefore, TGZo can be used as a substitute for microbial transglutaminase in the yogurt, even in the food industry.

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

Similar content being viewed by others

References

  1. Lorand L, Graham RM. Transglutaminases: crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 4: 140–156 (2003)

    Article  CAS  Google Scholar 

  2. Kieliszek M, Misiewicz A. Microbial transglutaminase and its application in the food industry. A review. Folia Microbiol. 59: 241–250 (2014)

    Article  CAS  Google Scholar 

  3. Jaros D, Partschefeld C, Henle T, Rohm H. Transglutaminase in dairy products: chemistry, physics, applications. J. Texture Stud. 37: 113–155 (2006)

    Article  Google Scholar 

  4. Lin YS, Chao ML, Liu CH, Chu WS. Cloning and expression of the transglutaminase gene from Streptoverticillium ladakanum in Streptomyces lividans. Process Biochem. 39: 591–598 (2004)

    Article  CAS  Google Scholar 

  5. Icekson I, Apelbaum A. Evidence for transglutaminase activity in plant tissue. Plant Physiol. 84: 972–974 (1987)

    Article  CAS  Google Scholar 

  6. Kang H, Cho YD. Purification and properties of transglutaminase from soybean (Glycine max) leaves. Biochem. Biophys. Res. Commun. 223: 288–292 (1996)

    Article  CAS  Google Scholar 

  7. Margosiak SA, Dharma A, Bruce-Carver MR, Gonzales AP, Louie D, Kuehn GD. Identification of the large subunit of ribulose 1, 5-bisphosphate carboxylase/oxygenase as a substrate for transglutaminase in Medicago sativa L.(Alfalfa). Plant Physiol. 92: 88–96 (1990)

    Article  CAS  Google Scholar 

  8. Serafini-Fracassini D, Del Duca S, Beninati S. Plant transglutaminases. Phytochemistry. 40: 355–365 (1995)

    Article  CAS  Google Scholar 

  9. Villalobos E, Santos M, Talavera D, Rodrıguez-Falcón M, Torné J. Molecular cloning and characterization of a maize transglutaminase complementary DNA. Gene. 336: 93–104 (2004)

    Article  CAS  Google Scholar 

  10. Signorini M, Beninati S, Bergamini CM. Identification of transglutaminase activity in the leaves of silver beet (Beta vulgaris L.). J. Plant Physiol. 137: 547–552 (1991)

    Article  CAS  Google Scholar 

  11. Della Mea M, Caparrós-Ruiz D, Claparols I, Serafini-Fracassini D, Rigau J. AtPng1p. The first plant transglutaminase. Plant Physiol. 135: 2046–2054 (2004)

    CAS  Google Scholar 

  12. Carvajal P, Gibert J, Campos N, Lopera O, Barberà E, Torné JM, Santos M. Activity of maize transglutaminase overexpressed in Escherichia coli inclusion bodies: An alternative to protein refolding. Biotechnol. Prog. 27: 232–240 (2011)

    Article  CAS  Google Scholar 

  13. Li H, Cui Y, Zhang L, Luo X, Fan R, Xue C, Wang S, Liu W, Zhang S, Jiao Y, Du M, Yi H, Han X. Production of a transglutaminase from Zea mays in Escherichia coli and its impact on yoghurt properties. Int. J. Dairy Technol. 68: 54–61 (2015)

    Article  Google Scholar 

  14. Li H, Cui Y, Zhang L, Yi H, Han X, Jiao Y, Du M, Fan R, Zhang S. Heterologous expression and purification of Zea mays transglutaminase in Pichia pastoris. Food Sci. and Biotech. 23: 1507–1513 (2014)

    Article  CAS  Google Scholar 

  15. Li H, Zhang L, Cui Y, Luo X, Xue C, Wang S. Expression of soluble recombinant transglutaminase from Zea mays in Pichia pastoris. World J. Microb. Biot. 29: 939–947 (2013)

    Article  CAS  Google Scholar 

  16. Li H, Zhang L, Cui Y, Luo X, Xue C, Wang S, Jiao Y, Zhang S, Liu W, Fan R. Characterization of recombinant Zea mays transglutaminase expressed in Pichia pastoris and its impact on full and non-fat yoghurts. J. Sci. Food Agric. 94: 1225–1230 (2014)

    Article  CAS  Google Scholar 

  17. Huang H, Yang P, Luo H, Tang H, Shao N, Yuan T, Wang Y, Bai Y, Yao B. High-level expression of a truncated 1, 3-1, 4-β-D-glucanase from Fibrobacter succinogenes in Pichia pastoris by optimization of codons and fermentation. Appl. Microbiol. Biotechnol. 78: 95–103 (2008)

    Article  CAS  Google Scholar 

  18. Liu S, Fang Y, Lv M, Wang S, Chen L. Optimization of the production of organic solvent-stable protease by Bacillus sphaericus DS11 with response surface methodology. Bioresource Technol. 101: 7924–7929 (2010)

    Article  CAS  Google Scholar 

  19. Kim HS, Lee AY, Jo JE, Moon BC, Chun JM, Choi G, Kim HK. Optimization of ultrasound-assisted extraction of quercitrin from Houttuynia cordata Thunb. using respon sesurface methodology and UPLC analysis. Food Sci. Biotechnol. 23: 1–7 (2014)

    Article  CAS  Google Scholar 

  20. Patil SA, Surwase SN, Jadhav SB, Jadhav JP. Optimization of medium using response surface methodology for L-DOPA production by Pseudomonas sp. SSA. Biochem. Eng. J. 74: 36–45 (2013)

    Article  CAS  Google Scholar 

  21. Roukas T, Niavi P, Kotzekidou P. A new medium for spore production of Blakeslea trispora using response surface methodology. World J. Microb. Biot. 27: 307–317 (2011)

    Article  CAS  Google Scholar 

  22. 22. Şanlı T, Sezgin E, Deveci O, Şenel E, Benli M. Effect of using transglutaminase on physical, chemical and sensory properties of set-type yoghurt. Food Hydrocolloid. 25: 1477–1481 (2011)

    Article  Google Scholar 

  23. Yüksel Z, Erdem Y. The influence of transglutaminase treatment on functional properties of set yoghurt. Int. J. Dairy Technol. 63: 86–97 (2010)

    Article  Google Scholar 

  24. Zhang L, Zhang L, Yi H, Du M, Ma C, Han X, Feng Z, Jiao Y, Zhang Y. Enzymatic characterization of transglutaminase from Streptomyces mobaraensis DSM 40587 in high salt and effect of enzymatic cross-linking of yak milk proteins on functional properties of stirred yogurt. J. Dairy Sci. 95: 3559–3568 (2012)

    Article  CAS  Google Scholar 

  25. Grossowicz N, Wainfan E, Borek E, Waelsch H. The enzymatic formation of hydroxamic acids from glutamine and asparagine. J. Biol. Chem. 187: 111–125 (1950)

    CAS  Google Scholar 

  26. Farnsworth JP, Li J, Hendricks GM, Guo MR. Effects of transglutaminase treatment on functional properties and probiotic culture survivability of goat milk yogurt. Small Ruminant Res. 65: 113–121 (2006)

    Article  Google Scholar 

  27. Mohana S, Shrivastava S, Divecha J, Madamwar D. Response surface methodology for optimization of medium for decolorization of textile dye Direct Black 22 by a novel bacterial consortium. Bioresource Technol. 99: 562–569 (2008)

    Article  CAS  Google Scholar 

  28. Kim S, Warburton S, Boldogh I, Svensson C, Pon L, d’Anjou M, Stadheim TA, Choi BK. Regulation of alcohol oxidase 1 (AOX1) promoter and peroxisome biogenesis in different fermentation processes in Pichia pastoris. J. Biotechnol. 166: 174–181 (2013)

    Article  CAS  Google Scholar 

  29. Antonenkov VD, Grunau S, Ohlmeier S, Hiltunen JK. Peroxisomes are oxidative organelles. Antioxid. Redox Signal 13: 525–537 (2010)

    Article  CAS  Google Scholar 

  30. Sakai Y, Oku M, van der Klei IJ, Kiel JA. Pexophagy: autophagic degradation of peroxisomes. BBA-Mol. Cell. Res. 1763: 1767–1775 (2006)

    CAS  Google Scholar 

  31. Erdmann R, Blobel G. Giant peroxisomes in oleic acid-induced Saccharomyces cerevisiae lacking the peroxisomal membrane protein Pmp27p. J. Cell Biol. 128: 509–523 (1995)

    Article  CAS  Google Scholar 

  32. Khatri NK, Hoffmann F. Impact of methanol concentration on secreted protein production in oxygen-limited cultures of recombinant Pichia pastoris. Biotechnol. Bioeng. 93: 871–879 (2006)

    Article  CAS  Google Scholar 

  33. Ozer B, Avni Kirmaci H, Oztekin S, Hayaloglu A, Atamer M. Incorporation of microbial transglutaminase into non-fat yogurt production. Int. Dairy J. 17: 199–207 (2007)

    Article  CAS  Google Scholar 

  34. Gauche C, Tomazi T, Barreto PLM, Ogliari PJ, Bordignon-Luiz MT. Physical properties of yoghurt manufactured with milk whey and transglutaminase. LWT- Food Sci. Technol. 42: 239–243 (2009)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Nature Science Foundation of China (Grant No. 31601496 and 31301545), China Postdoctoral Science Foundation (Grant No. 2014M560244), International Postdoctoral Exchange Fellowship Program of China (Grant No. 20150082) and Heilongjiang Postdoctoral Foundation (Grant No. LBH-Z13042).

Author information

Authors and Affiliations

  1. School of Food and Engineering and Biological Technology, Tianjin University of Science & Technology, Tianjin, 300457, China

    Hongbo Li & Jinghua Yu

  2. School of Food Science and Engineering, Harbin Institute of Technology, Harbin, 150090, Heilongjiang, China

    Yanhua Cui, Lanwei Zhang & Hui Liu

  3. College of Food Science, Northeast Agricultural University, Harbin, 150030, Heilongjiang, China

    Lili Zhang

Authors
  1. Hongbo Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yanhua Cui
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lanwei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lili Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hui Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jinghua Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lanwei Zhang.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, H., Cui, Y., Zhang, L. et al. Optimization of recombinant Zea mays transglutaminase production and its influence on the functional properties of yogurt. Food Sci Biotechnol 26, 723–730 (2017). https://doi.org/10.1007/s10068-017-0083-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10068-017-0083-5

Keywords

Search

Navigation