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Economical production of isomaltulose from agricultural residues in a system with sucrose isomerase displayed on Bacillus subtilis spores

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Abstract

A safe, efficient, environmentally friendly process for producing isomaltulose is needed. Here, the biocatalyst, sucrose isomerase (SIase) from Erwinia rhapontici NX-5, displayed on the surface of Bacillus subtilis 168 spores (food-grade strain) was applied for isomaltulose production. The anchored SIase showed relatively high bioactivity, suggesting that the surface display system using CotX as the anchoring protein was successful. The stability of the anchored SIase was also significantly better. Thermal stability analysis showed that 80% of relative activity was retained after incubation at 40 °C and 45 °C for 60 min. To develop an economical industrial fermentation medium, untreated beet molasses (30 g/L) and cold-pressed soybean powder (50 g/L) were utilised as the main broth components for SIase pilot-scale production. Under the optimal conditions, the productive spores converted 92% of sucrose after 6 h and the conversion rate was 45% after six cycles. Isomaltulose production with this system using the agricultural residues, untreated beet molasses and soybean powder, as substrates is cost-effective and environmentally friendly and can help to overcome issues due to the genetic background.

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References

  1. Sachdev R (2018) Sugar substitutes and dental health. Int J Basic Clin Pharmacol 7:1667

    Article  Google Scholar 

  2. 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 Biotechnol 98:6569–6582

    Article  CAS  Google Scholar 

  3. Carvalho F, Fernandes P (2019) Enzymes in Sweeteners production. Green Bio-processes. Springer, Singapore, pp 151–179

    Google Scholar 

  4. Zhan Y, Xu Z, Li S, Liu X, Xu L, Feng X, Xu H (2014) Coexpression of beta-d-galactosidase and l-arabinose isomerase in the production of d-tagatose: a functional sweetener. J Agric Food Chem 62:2412–2417

    Article  CAS  Google Scholar 

  5. He W, Mu W, Jiang B, Yan X, Zhang T (2016) Food-grade expression of d-psicose 3-epimerase with tandem repeat genes in Bacillus subtilis. J Agric Food Chem 64:5701–5707

    Article  CAS  Google Scholar 

  6. Yamashita K, Kawai K, Itakura M (1984) Effects of fructo-oligosaccharides on blood glucose and serum lipids in diabetic subjects. Nutr Res 4:961–966

    Article  CAS  Google Scholar 

  7. Cheetham PSJ, Imber CE, Isherwood J (1982) the formation of isomaltulose by immobilized Erwinia rhapontici. Nature 299:628–631

    Article  CAS  Google Scholar 

  8. Buchowski M, Fleddermann M, Rauh-Pfeiffer A, Demmelmair H, Holdt L, Teupser D, Koletzko B (2016) Effects of a follow-on formula containing isomaltulose (Palatinose™) on metabolic response, acceptance, tolerance and Safety in infants: a randomized-controlled trial. PLoS ONE 11:e0151614

    Article  Google Scholar 

  9. Sporns P, Plhak L, Friedrich J (1992) Alberta honey composition. Food Res Int 25:93–100

    Article  CAS  Google Scholar 

  10. Rastogi H, Bhatia S (2019) Future prospectives for enzyme technologies in the food industry. In: Enzymes in food biotechnology. Academic Press, pp 845–860

  11. Li S, Cai H, Qing Y, Ren B, Xu H, Zhu H, Yao J (2011) Cloning and characterization of a sucrose isomerase from Erwinia rhapontici NX-5 for isomaltulose hyperproduction. Appl Biochem Biotechnol 163:52–63

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  13. Ravaud S, Watzlawick H, Haser R, Mattes R, Aghajari N (2005) Overexpression, purification, crystallization and preliminary diffraction studies of theProtaminobacter rubrumsucrose isomerase SmuA. Acta Crystallogr, Sect F Struct Biol Cryst Commun 62:74–76

    Article  Google Scholar 

  14. 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

    Article  CAS  Google Scholar 

  15. 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

    Article  CAS  Google Scholar 

  16. Xu Z, Li S, Li J, Li Y, Feng X, Wang R, Xu H, Zhou J (2013) The structural basis of Erwinia rhapontici isomaltulose synthase. PLoS ONE 8:e74788

    Article  CAS  Google Scholar 

  17. Zhang P, Wang ZP, Liu S, Wang YL, Zhang ZF, Liu XM, Du YM, Yuan XL (2019) Overexpression of secreted sucrose isomerase in Yarrowia lipolytica and its application in isomaltulose production after immobilization. Int J Biol Macromol 121:97–103

    Article  CAS  Google Scholar 

  18. Wu L, Liu Y, Chi B, Xu Z, Feng X, Li S, Xu H (2015) An innovative method for immobilizing sucrose isomerase on epsilon-poly-L-lysine modified mesoporous TiO2. Food Chem 187:182–188

    Article  CAS  Google Scholar 

  19. He Y-H, Xiang Y, Yang D-C, Guan Z (2016) Combining enzyme and photoredox catalysis for aminoalkylation of indoles via a relay catalysis strategy in one pot. Green Chem 18:5325–5330

    Article  CAS  Google Scholar 

  20. Ward K, Xi J, Stuckey DC (2016) Immobilization of enzymes using non-ionic colloidal liquid aphrons (CLAs): Activity kinetics, conformation, and energetics. Biotechnol Bioeng 113:970–978

    Article  CAS  Google Scholar 

  21. Kim D, Ku S (2018) Bacillus Cellulase molecular cloning, expression, and surface display on the outer membrane of Escherichia coli. Molecules 23

  22. Liu Y, Li S, Xu H, Wu L, Xu Z, Liu J, Feng X (2014) Efficient production of d-tagatose using a food-grade surface display system. J Agric Food Chem 62:6756–6762

    Article  CAS  Google Scholar 

  23. Lee GY, Jung JH, Seo DH, Hansin J, Ha SJ, Cha J, Kim YS, Park CS (2011) Isomaltulose production via yeast surface display of sucrose isomerase from Enterobacter sp. FMB-1 on Saccharomyces cerevisiae. Bioresour Technol 102(19):9179–9184

    Article  CAS  Google Scholar 

  24. Park J-Y, Jung J-H, Seo D-H, Ha S-J, Yoon J-W, Kim Y-C, Shim J-H, Park C-S (2010) Microbial production of palatinose through extracellular expression of a sucrose isomerase from Enterobacter sp. FMB-1 in Lactococcus lactis MG1363. Biores Technol 101:8828–8833

    Article  CAS  Google Scholar 

  25. Chauhan PS, Jha B (2018) Pilot scale production of extracellular thermo-alkali stable laccase from Pseudomonas sp. S2 using agro waste and its application in organophosphorous pesticides degradation. J Chem Technol Biotechnol 93:1022–1030

    Article  CAS  Google Scholar 

  26. Ergun M, Mutlu SF (2000) Application of a statistical technique to the production of ethanol from sugar beet molasses by Saccharomyces cerevisiae. Biores Technol 73:251–255

    Article  CAS  Google Scholar 

  27. Valli V, Gomez-Caravaca AM, Di Nunzio M, Danesi F, Caboni MF, Bordoni A (2012) Sugar cane and sugar beet molasses, antioxidant-rich alternatives to refined sugar. J Agric Food Chem 60:12508–12515

    Article  CAS  Google Scholar 

  28. Liu T, Bessembayeva L, Chen J, Wei L-J, Hua Q (2019) Development of an economical fermentation platform for enhanced ansamitocin P-3 production in Actinosynnema pretiosum. Bioresour Bioprocess 6(1):1

    Article  Google Scholar 

  29. Wang C, Xu H, Zhang Y, Wu S, Chen D, Qian G, Hu B, Fan J (2019) Optimization of culture conditions for promoting heat-stable antifungal factor production level in Lysobacter enzymogenes. FEMS Microbiol Lett

  30. Ning D, Leng X, Li Q, Xu W (2011) Surface-displayed VP28 on Bacillus subtilis spores induce protection against white spot syndrome virus in crayfish by oral administration. J Appl Microbiol 111:1327–1336

    Article  CAS  Google Scholar 

  31. Li G, Tang Q, Chen H, Yao Q, Ning D, Chen K (2011) Display of Bombyx mori nucleopolyhedrovirus GP64 on the Bacillus subtilis spore coat. Curr Microbiol 62:1368–1373

    Article  CAS  Google Scholar 

  32. Zhang D, Feng X, Zhou Z, Zhang Y, Xu H (2012) Economical production of poly(gamma-glutamic acid) using untreated cane molasses and monosodium glutamate waste liquor by Bacillus subtilis NX-2. Bioresour Technol 114:583–588

    Article  CAS  Google Scholar 

  33. Xu X, Gao C, Zhang X, Che B, Ma C, Qiu J, Tao F, Xu P (2011) Production of N-acetyl-D-neuraminic acid by use of an efficient spore surface display system. Appl Environ Microbiol 77:3197–3201

    Article  CAS  Google Scholar 

  34. Wu L, Wu S, Qiu J, Xu C, Li S, Xu H (2017) Green synthesis of isomaltulose from cane molasses by Bacillus subtilis WB800-pHA01-palI in a biologic membrane reactor. Food Chem 229:761–768

    Article  CAS  Google Scholar 

  35. Harwood CR, Wipat A (1996) Sequencing and functional analysis of the genome of Bacillus subtilis strain 168. FEBS Lett 389:84–87

    Article  CAS  Google Scholar 

  36. Yang C, Song C, Freudl R, Mulchandani A, Qiao C (2010) Twin-arginine translocation of methyl parathion hydrolase in Bacillus subtilis. Environ Sci Technol 44:7607–7612

    Article  CAS  Google Scholar 

  37. Chityala S, Venkata Dasu V, Ahmad J, Prakasham RS (2015) High yield expression of novel glutaminase free l-asparaginase II of Pectobacterium carotovorum MTCC 1428 in Bacillus subtilis WB800N. Bioprocess Biosyst Eng 38:2271–2284

    Article  CAS  Google Scholar 

  38. Zhang D, Li X, Zhang LH (2002) Isomaltulose synthase from Klebsiella sp. strain LX3: gene cloning and characterization and engineering of thermostability. Appl Environ Microbiol 68:2676–2682

    Article  CAS  Google Scholar 

  39. Cha J, Jung JH, Park SE, Cho MH, Seo DH, Ha SJ, Yoon JW, Lee OH, Kim YC, Park CS (2009) Molecular cloning and functional characterization of a sucrose isomerase (isomaltulose synthase) gene from Enterobacter sp. FMB-1. J Appl Microbiol 107:1119–1130

    Article  CAS  Google Scholar 

  40. Kawaguti HY, Celestino ÉM, Moraes ALL, Yim DK, Yamamoto LK, Sato HH (2010) Characterization of a glucosyltransferase from Erwinia sp. D12 and the conversion of sucrose into isomaltulose by immobilized cells. Biochem Eng J 48:211–217

    Article  CAS  Google Scholar 

  41. Wu L, Qiu J, Wu S, Liu X, Liu C, Xu Z, Li S, Xu H (2016) Bioinspired production of antibacterial sucrose isomerase-sponge for the synthesis of isomaltulose. Adv Synth Catal 358(24):4030–4040

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key R&D Program of China [Grant no. 2017YFD0400403], National Natural Science Foundation of China [Grant no. 21878152], Natural Science Foundation of Jiangsu Province [Grant no. BK20160985], Jiangsu Synergetic Innovation Center for Advanced Bio-Manufacture [Grant no. XTB1804], State Key Laboratory of Materials-Oriented Chemical Engineering [Grant no. ZK201606], Six Talent Peaks Project in Jiangsu Province [Grant no. SWYY-027], and Qing Lan Project. The sponsors had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; and in the decision to submit the article for publication.

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  1. Yijing Zhan and Ping Zhu had equal contributions to this work.

Authors and Affiliations

  1. State Key Laboratory of Materials-Oriented Chemical Engineering, Nanjing Tech University, 30 Puzhu South Road, Nanjing, 211816, People’s Republic of China

    Yijing Zhan, Ping Zhu, Jinfeng Liang, Zheng Xu, Yi Liu, Hong Xu & Sha Li

  2. College of Food Science and Light Industry, Nanjing Tech University, 30 Puzhu South Road, Nanjing, 211816, People’s Republic of China

    Yijing Zhan, Ping Zhu, Jinfeng Liang, Zheng Xu, Yi Liu, Hong Xu & Sha Li

  3. Nanjing Shineking Biotech Co., Ltd, Nanjing, 210061, People’s Republic of China

    Xiaohai Feng

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  1. Yijing Zhan
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Zhan, Y., Zhu, P., Liang, J. et al. Economical production of isomaltulose from agricultural residues in a system with sucrose isomerase displayed on Bacillus subtilis spores. Bioprocess Biosyst Eng 43, 75–84 (2020). https://doi.org/10.1007/s00449-019-02206-6

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  • DOI: https://doi.org/10.1007/s00449-019-02206-6

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