Skip to main content

Immobilization of Serratia plymuthica by ionic gelation and cross-linking with transglutaminase for the conversion of sucrose into isomaltulose

Abstract

Isomaltulose is an alternative sugar obtained from sucrose using some bacteria producing glycosyltransferase. This work aimed to optimize conditions for the immobilization of Serratia plymuthica through ionic gelation and cross-linking by transglutaminase using the sequential experimental strategy for the conversion of sucrose into isomaltulose. The effect of five variables (concentrations of cell mass, alginate, gelatin, transglutaminase, and calcium chloride) was studied, as well as the interactions between them on the matrix composition for the S. plymuthica immobilization. Three experimental designs were used to optimize the concentrations of each variable to obtain higher concentration of isomaltulose. A high conversion of sucrose into isomaltulose (71.04%) was obtained by the cells immobilized in a matrix composed of alginate (1.7%), CaCl2 (0.25 mol/L), gelatin (0.5%), transglutaminase (3.5%) and cell mass (33.5%). As a result, the transglutaminase application as a cross-linking agent improved the immobilization of Serratia plymuthica cells and the conversion of sucrose into isomaltulose.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

Availability of data and material

The data supporting the results of this study will be made available by the corresponding author, upon reasonable request.

References

  1. 1.

    Adhikari S (2019) In: Kuddus M (ed) Enzymes in food biotechnology: production, applications, and future prospects, 1st edn. Elsevier, Amsterdãm

  2. 2.

    Bahry H, Abdalla R, Pons A et al (2019) Optimization of lactic acid production using immobilized Lactobacillus rhamnosus and carob pod waste from the Lebanese food industry. J Biotechnol 306:81–88

    CAS  Article  Google Scholar 

  3. 3.

    Bhujbal SV, Paredes-Juarez GA, Niclou SP, de Vos P (2014) Factors influencing the mechanical stability of alginate beads applicable for immunoisolation of mammalian cells. J Mech Behav Biomed Mater 37:196–208

    CAS  Article  Google Scholar 

  4. 4.

    Cantone S, Ferrario V, Corici L, Ebert C, Fattor D, Spizzo P, Gardossi L (2013) Efficient immobilization of industrial biocatalysts: Criteria and constraints for the selection of organic polymeric carriers and immobilization methods. Chem Soc Rev 42:6262–6276

    CAS  Article  Google Scholar 

  5. 5.

    Chibata I, Tosa T (1983) In: Chibata I (ed) Applied biochemistry and bioengineering, 4th edn. Academic Press, Cambridge

  6. 6.

    Contesini FJ, Ibarguren C, Grosso CRF, Carvalho PO, Sato HH (2012) Immobilization of glucosyltransferase from Erwinia sp. using two different techniques. J Biotechnol 158:137–143

    CAS  Article  Google Scholar 

  7. 7.

    Contesini FJ, Carvalho PO, Grosso CRF, Sato HH (2013) Single-step purification, characterization and immobilization of a sucrose isomerase from Erwinia sp. Biocatal Agric Biotechnol 2:322–327

    Article  Google Scholar 

  8. 8.

    de Oliva-Neto P, Menão PTP (2009) Isomaltulose production from sucrose by Protaminobacter rubrum immobilized in calcium alginate. Bioresour Technol 100:4252–4256

    Article  Google Scholar 

  9. 9.

    de Oliveira RL, Dias JL, da Silva OS, Porto TS (2018) Immobilization of pectinase from Aspergillus aculeatus in alginate beads and clarification of apple and umbu juices in a packed bed reactor. Food Bioprod Process 109:9–18

    Article  Google Scholar 

  10. 10.

    Evingür GA, Kaygusuz H, Erim FB, Pekcan Ö (2014) Effect of calcium ion concentration on small molecule desorption from alginate beads. J Macromol Sci B 53:1157–1167

    Article  Google Scholar 

  11. 11.

    Gaspar ALC, de Góes-Favoni SP (2015) Action of microbial transglutaminase (MTGase) in the modification of food proteins: A review. Food Chem 171:315–322

    CAS  Article  Google Scholar 

  12. 12.

    Goh CH, Heng PWS, Chan LW (2012) Alginates as a useful natural polymer for microencapsulation and therapeutic applications. Carbohydr Polym 88:1–12

    CAS  Article  Google Scholar 

  13. 13.

    Gong P, Di W, Yi H, Sun J, Zhang L, Han X (2019) Improved viability of spray-dried Lactobacillus bulgaricus sp1.1 embedded in acidic-basic proteins treated with transglutaminase. Food Chem 281:204–212

    CAS  Article  Google Scholar 

  14. 14.

    Hellmers F, Takors R, Thum O (2018) Robust enzyme immobilizates for industrial isomalt production. Mol Catal 445:293–298

    CAS  Article  Google Scholar 

  15. 15.

    Kawaguti HY, Manrich E, Sato HH (2006) Production of isomaltulose using Erwinia sp. D12 cells: culture medium optimization and cell immobilization in alginate. Biochem Eng J 29:270–277

    CAS  Article  Google Scholar 

  16. 16.

    Kawaguti HY, Sato HH (2010) Isomaltulose production by free cells of Serratia plymuthica in a batch process. Food Chem 120:789–793

    CAS  Article  Google Scholar 

  17. 17.

    Kawaguti HY, Carvalho PH, Figueira JA, Sato HH (2011) Immobilization of Erwinia sp. D12 cells in alginate-gelatin matrix and conversion of sucrose into isomaltulose using response surface methodology. Enzyme Res 2011:1–8

    Article  Google Scholar 

  18. 18.

    Kim Y, Koo BS, Lee HC, Yoon Y (2015) Improved production of isomaltulose by a newly isolated mutant of Serratia sp. cells immobilized in calcium alginate. Can J Microbiol 61:193–199

    CAS  Article  Google Scholar 

  19. 19.

    Kurozawa LE, Hubinger MD (2017) Hydrophilic food compounds encapsulation by ionic gelation. Curr Opin Food Sci 15:50–55

    Article  Google Scholar 

  20. 20.

    Krastanov A, Blazheva D, Stanchev V (2007) Sucrose conversion into palatinose with immobilized Serratia plymuthica cells in a hollow-fibre bioreactor. Process Biochem 42:1655–1659

    CAS  Article  Google Scholar 

  21. 21.

    Li X, Zhang D, Chen F, Ma J, Dong Y, Zhang L (2004) Klebsiella singaporensis sp. nov., a novel isomaltulose-producing bacterium. Int J Syst Evol Micr 54:2131–2136

    CAS  Article  Google Scholar 

  22. 22.

    Macedo JA, Sette LD, Sato HH (2011) Purification and characterization of a new transglutaminase from Streptomyces sp. isolated in Brazilian soil. J Food Biochem 35:1361–1372

    CAS  Article  Google Scholar 

  23. 23.

    Maeda A, Miyagawa JI, Miuchi M et al (2013) Effects of the naturally-occurring disaccharides, palatinose, and sucrose, on incretin secretion in healthy non-obese subjects. J Diabetes Investig 4:281–286

    CAS  Article  Google Scholar 

  24. 24.

    Martins E, Poncelet D, Rodrigues RC, Renard D (2017) Oil encapsulation techniques using alginate as encapsulating agent: applications and drawbacks. J Microencapsul 34:754–771

    CAS  Article  Google Scholar 

  25. 25.

    Mu W, Li W, Wang X, Zhang T, Jiang B (2014) Current studies on sucrose isomerase and biological isomaltulose production using sucrose isomerase. Appl Microbiol Biot 98:6569–6582

    CAS  Article  Google Scholar 

  26. 26.

    Nawawi NN, Hashim Z, Rahman RA et al (2020) Entrapment of porous cross-linked enzyme aggregates of maltogenic amylase from Bacillus lehensis G1 into calcium alginate for maltooligosaccharides synthesis. Int J Biol Macromol 150:80–89

    CAS  Article  Google Scholar 

  27. 27.

    Orsi DC, Sato HH (2016) Isomaltulose production using free and immobilized Serratia plymuthica cells. Afr J Biotechol 15:835–842

    CAS  Article  Google Scholar 

  28. 28.

    Pathak TS, Yun Jung-Ho, Lee J, Paeng Ki-Jung (2010) Effect of calcium ion (cross-linker) concentration on porosity, surface morphology and thermal behavior of calcium alginates prepared from algae (Undaria pinnatifida). Carbohydr Polym 7:633–639

  29. 29.

    Rehman HU, Aman A, Silipo A et al (2013) Degradation of complex carbohydrate: immobilization of pectinase from Bacillus licheniformis KIBGE-IB21 using calcium alginate as a support. Food Chem 139:1081–1086

    Article  Google Scholar 

  30. 30.

    Rodrigues MI, Iemma AF (2014) Experimental design and process optimization. Cárita, Campinas, São Paulo, Brazil

    Book  Google Scholar 

  31. 31.

    Rodrigues FJ, Omura MH, Cedran MF, Dekker RFH, Barbosa-Dekker AM, Garcia S (2017) Effect of natural polymers on the survival of Lactobacillus casei encapsulated in alginate microspheres. J Microencapsul 34:431–439

    CAS  Article  Google Scholar 

  32. 32.

    Rodrigues FJ, Cedran MF, Bicas JL, Sato HH (2020) Encapsulated probiotic cells: relevant techniques, natural sources as encapsulating materials and food applications—a narrative review. Food Res Int 137:109682

    CAS  Article  Google Scholar 

  33. 33.

    Sawale PD, Shendurse AM, Mohan MS, Patil GR (2017) Isomaltulose (Palatinose)—an emerging carbohydrate. Food Biosci 18:46–52

    CAS  Article  Google Scholar 

  34. 34.

    Shyam S, Ramadas A, Chang SK (2018) Isomaltulose: Recent evidence for health benefits. J Funct Foods 48:173–178

    CAS  Article  Google Scholar 

  35. 35.

    Soukoulis C, Yonekura L, Heng-Hui G, Behboudi-Jobbehdar S, Parmenter C, Fisk I (2014) Probiotic edible films as a new strategy for developing functional bakery products: the case of pan bread. Food Hydrocoll 39:231–241

    CAS  Article  Google Scholar 

  36. 36.

    Tan WSK, Tan SY, Henry CJ (2017) Ethnic variability in glycemic response to sucrose and isomaltulose. Nutrients 9:1–7

    Google Scholar 

  37. 37.

    Véronèse T, Perlot P (1999) Mechanism of sucrose conversion by the sucrose isomerase of Serratia plymuthica ATCC 15928. Enzyme Microb Technol 24:263–269

    Article  Google Scholar 

  38. 38.

    Xiao Y, Han C, Yang H, Liu M, Meng X, Liu B (2020) Layer (whey protein isolate)-by-layer (xanthan gum) microencapsulation enhances survivability of L. bulgaricus and L. paracasei under simulated gastrointestinal juice and thermal conditions. Int J Biol Macromol 148:238–247

    CAS  Article  Google Scholar 

  39. 39.

    Yushkova ED, Nazarova EA, Matyuhina AV, Noskova AO, Shavronskaya DO, Vinogradov VV, Krivoshapkina EF (2019) Application of immobilized enzymes in food industry. J Agr Food Chem 67:11553–11567

    CAS  Article  Google Scholar 

Download references

Funding

This work was supported in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Brazil (CAPES)—Finance Code 001 (PROEX process number 23038.000795/2018-61). The authors would like to thank the Department of Food Science and Nutrition, School of Food Engineering, University of Campinas.

Author information

Affiliations

Authors

Contributions

All authors contributed to the development of this research, as follows: PHC: Conceptualization, methodology, formal analysis, investigation, data curation, writing—original draft, writing—review and editing. HYK: Methodology, formal analysis, investigation, and data curation. WFCS: Conceptualization, investigation, writing—review and editing. HHS: Conceptualization, resources, writing—original draft, writing—review and editing, supervision, project administration, and funding acquisition.

Corresponding author

Correspondence to Weysser Felipe Cândido de Souza.

Ethics declarations

Conflict of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Carvalho, P.H., Kawaguti, H.Y., de Souza, W.F.C. et al. Immobilization of Serratia plymuthica by ionic gelation and cross-linking with transglutaminase for the conversion of sucrose into isomaltulose. Bioprocess Biosyst Eng 44, 1109–1118 (2021). https://doi.org/10.1007/s00449-021-02513-x

Download citation

Keywords

  • Serratia plymuthica
  • Glycosyltransferases
  • Immobilization
  • Ionic gelation