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Inulinase-expressing microorganisms and applications of inulinases

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Abstract

In this review article, inulinase-expressing microorganisms and its potential applications in transformation of inulin into very-high-fructose syrup, bioethanol, and inulooligosaccharides are overviewed. In the past 10 years, many new inulinase producers have been obtained and many genes encoding inulinases from different microorganisms have been cloned and characterized. Some novel processes for exoinulinase overproduction have been developed for bioethanol production and ultra-high-fructose syrup. The endoinulinases have also been used for production of inulooligosaccharides from inulin and inulin-containing materials.

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References

  • Barranco-Florido E, Garcia-Garibay M, Go’mez-Ruiz L, Azaola A (2001) Immobilization system of Kluyveromyces marxianus cells in barium alginate for inulin hydrolysis. Proc Biochem 37:513–519

    Article  Google Scholar 

  • Bender JP, Mazutti MA, Treichel H, Di Luccio M (2006) Inulinase production by Kluyveromyces marxianus NRRL Y-7571 using solid state fermentation. Appl Biochem Biotechnol 32:951–958

    Article  Google Scholar 

  • Bergkamp RJ, Bootsman TC, Toschka HY, Mooren AT, Kox L, Verbakel JM, Geerse RH, Planta RJ (1993) Expression of an alpha-galactosidase gene under control of the homologous inulinase promoter in Kluyveromyces marxianus. Appl Microbiol Biotechnol 40:309–317

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Wang JH, Li DS (2007) Optimization of solid-state medium for the production of inulinase by Kluyveromyces S120 using response surface methodology. Biochem Eng J 34:179–184

    Article  CAS  Google Scholar 

  • Cruz-Guerrero AE, Olvera JL, Garcia-Garibay M, Gomez-Ruiz L (2006) Inulinase-hyperproducing strains of Kluyveromyces sp. isolated from aguamiel (Agave sap) and pulque. World J Microbiol Biotechnol 22:115–117

    Article  CAS  Google Scholar 

  • de Paula FC, Cazetta ML, Monti R, Contiero J (2008) Sucrose hydrolysis by gelatin-immobilized inulinase from Kluyveromyces marxianus var. bulgaricus. Food Chem 111:691–695

    Article  CAS  Google Scholar 

  • Gao LM, Chi ZM, Sheng J, Ni XM, Wang L (2007a) Single-cell protein production from Jerusalem artichoke extract by a recently isolated marine yeast Cryptococcus aureus G7a and its nutritive analysis. Appl Microbiol Biotechnol 77:825–832

    Article  CAS  PubMed  Google Scholar 

  • Gao LM, Chi ZM, Sheng J, Wang L, Li J, Gong F (2007b) Inulinase-producing marine yeasts: evaluation of their diversity and inulin hydrolysis by their crude enzymes. Microbiol Ecol 54:722–729

    Article  CAS  Google Scholar 

  • Gill PK, Manhas RK, Singh P (2006) Hydrolysis of inulin by immobilized thermostable extracellular exoinulinase from Aspergillus fumigatus. J Food Eng 76:369–375

    Article  CAS  Google Scholar 

  • Gong F, Sheng J, Chi ZM, Li J (2007) Inulinase production by a marine yeast Pichia guilliermondii and inulin hydrolysis by the crude inulinase. J Indu Microbiol Biotechnol 34:179–185

    Article  CAS  Google Scholar 

  • Gong F, Chi ZM, Sheng J, Li J, Wang XH (2008) Purification and characterization of extracellular inulinase from a marine yeast Pichia guilliermondii and Inulin hydrolysis by the purified inulinase. Biotechnol Bioproc Eng 13:533–539

    Article  CAS  Google Scholar 

  • Guo N, Gong F, Chi ZM, Sheng J, Li J (2008) Enhanced inulinase production in solid state fermentation by a mutant of the marine yeast Pichia guilliermondii using surface response methodology and inulin hydrolysis. J Ind Microbiol Biotechnol doi:https://doi.org/10.1007/s10295-008-05192

  • Kang SI, Chang YJ, Oh SJ, Kim SI (1998) Purification and properties of an endo-inulinase from an Arthrobacter sp. Biotechnol Lett 20:983–986

    Article  CAS  Google Scholar 

  • Kango N (2008) Production of inulinase using tap roots of dandelion (Taraxacum officinale) by Aspergillus niger. J Food Eng 85:473–478

    Article  CAS  Google Scholar 

  • Kim CH, Rhee SK (1989) Fructose production from Jerusalem artichoke by inulinase immobilized on chin. Biotechnol Lett 2(3):201–206

    Article  Google Scholar 

  • Kim DH, Choi YJ, Song SK, Yun JW (1997) Production of inulo-oligosaccharides using endo-inulinase from a Pseudomonas sp. Biotechnol Lett 19:369–371

    Article  CAS  Google Scholar 

  • Kim HS, Lee DW, Ryu EJ, Uhm TB, Yang MS, Kim JB, Chae KS (1999) Expression of the INU2 gene for an endoinulinase of Aspergillus ficuum in Saccharomyces cerevisiae. Biotechnol Lett 21:621–623

    Article  CAS  Google Scholar 

  • Kim KY, Koo BS, Jo D, Kim SI (2004) Cloning, expression and purification of exo-inulinase from Bacillus sp. Snu-7. J Microbiol Biotechnol 14(2):344–349

    CAS  Google Scholar 

  • Kim HC, Kim HJ, Choi WB, Nam SW (2006) Inulooligosaccharide production from inulin by Saccharomyces cerevisiae strain displaying cell-surface endoinulinase. J Microbiol Biotechnol 16(3):360–367

    Article  CAS  Google Scholar 

  • Kim KY, Nascimento AS, Golubev AM, Polikarpov I, Kim CS, Kang S, Kim S (2008) Catalytic mechanism of inulinase from Arthrobacter sp. S37. Biochem Biophys Res Commun 371:600–605

    Article  CAS  PubMed  Google Scholar 

  • Kushi RT, Monti R, Contiero J (2000) Production, purification and characterization of an extracellular inulinase came from Kluyveromyces marxianus var. bulgaricus. J Ind Microbiol Biotechnol 25:63–69

    Article  CAS  Google Scholar 

  • Kwon YM, Kim HY, Choi YJ (2000) Cloning and characterization of Pseudomonas mucidolens exoinulinase. J Microbiol Biotechnol 10(2):238–243

    CAS  Google Scholar 

  • Kwon HJ, Jeon SJ, You DJ, Kim KH, Jeong YK, Kim YH, Kim YM, Kim BW (2003) Cloning and characterization of an exoinulinase from Bacillus polymyxa. Biotechnol Lett 25:155–159

    Article  CAS  PubMed  Google Scholar 

  • Laloux O, Cassart JP, Delcour J, Van Beeumen J, Vandenhaute J (1991) Cloning and sequencing of the inulinase gene of Kluyveromyces marxianus var. marxianus ATCC 12424. FEBS Lett 289:64–68

    Article  CAS  PubMed  Google Scholar 

  • Lo’pez-Molina D, Navarro-Martinez MD, Melgarejo FR, Hiner ANP, Chazarra S, Rodriguez-Lo’pez JN (2005) Molecular properties and prebiotic effect of inulin obtained from artichoke (Cynara scolymus L.). Phytochem 66:1476–1484

    Article  CAS  Google Scholar 

  • Mazutti M, Bender JP, Treichel H, Luccio MD (2006) Optimization of inulinase production by solid-state fermentation using sugarcane bagasse as substrate. Enzyme Microb Technol 39:56–59

    Article  CAS  Google Scholar 

  • Nagem RAP, Rojas AL, Golubev AM, Korneeva OS, Eneyskaya EV, Kulminskaya AA, Neustroev KN, Polikarpov I (2004) Crystal structure of exo-inulinase from Aspergillus awamori: the enzyme fold and structural determinants of substrate recognition. J Mol Biol 344:471–480

    Article  CAS  PubMed  Google Scholar 

  • Nakamura T, Ogata Y, Hamada S, Ohta K (1996) Ethanol production from Jerusalem artichoke tubers by Aspergillus niger and Saccharomyces cerevisiae. J Fermen Bioeng 81:564–566

    Article  CAS  Google Scholar 

  • Nakamura T, Shitara A, Matsuda S, Matsuo T, Suiko M, Ohta K (1997) Production, purification and properties of an endoinulinase of Penicillium sp. TN-88 that liberates inulotriose. J Fermen Bioeng 84:313–318

    Article  CAS  Google Scholar 

  • Nakamura T, Ogata Y, Shitara A, Nakamura A, Ohta K (1995) Continuous production of fructose syrups from inulin by immobilized inulinase from Aspergillus niger mutant 817. J Fermen Bioeng 80:164–169

    Article  CAS  Google Scholar 

  • Ni XM, Yue LX, Chi ZM, Li J, Wang XH, Madzak C (2008) Alkaline protease gene cloning from the marine yeast Aureobasidium pullulans HN2-3 and the protease surface display on Yarrowia lipolytica for bioactive peptide production. Mar Biotechnol. doi:https://doi.org/10.1007/s10126-008-9122-9

    Article  PubMed  CAS  Google Scholar 

  • Pandey A, Soccol CR, Selvakumar P, Soccol VT, Krieger N, Jose D (1999) Recent developments in microbial inulinases, its production, properties and industrial applications. Appl Biochem Biotechnol 81:35–52

    Article  CAS  PubMed  Google Scholar 

  • Remize F, Schorr-Galindo S, Guiraud JP, Dequin S, Blondin B (1998) Construction of a flocculating yeast for fructose production from inulin. Biotechnol Lett 20:313–318

    Article  CAS  Google Scholar 

  • Rocha JR, Catana R, Ferreira BS, Cabral JMS, Fernandes P (2006) Design and characterization of an enzyme system for inulin hydrolysis. Food Chem 95:77–82

    Article  CAS  Google Scholar 

  • Ronkart SN, Blecker CS, Fourmanoir H, Fougnies C, Deroanne C, Herck JCV, Paquot M (2007) Isolation and identification of inulooligosaccharides resulting from inulin hydrolysis. Anal Chim Acta 604:81–87

    Article  CAS  PubMed  Google Scholar 

  • Rouwenhorst RJ, Hensing M, Verbakel J, Scheffers WA, Van Dijken JP (1999) Structure and properties of the extracellular inulinase of Kluyveromyces marxianus CBS 6556. Appl Environ Microbiol 11:3337–3345

    Google Scholar 

  • Sanchez OJ, Cardona CA (2008) Trends in biotechnological production of fuel ethanol from different feedstocks. Biores Technol 99:5270–5295

    Article  CAS  Google Scholar 

  • Selvakumar P, Pandey A (1999) Solid state fermentation for the synthesis of inulinase from Staphylococcus sp. and Kluyveromyces marxianus. Proc Biochem 34:851–855

    Article  CAS  Google Scholar 

  • Sheng J, Chi ZM, Li J, Gao LM, Gong F (2007) Inulinase production by the marine yeast Cryptococcus aureus G7a and inulin hydrolysis by the crude inulinase. Proc Biochem 42:805–811

    Article  CAS  Google Scholar 

  • Sheng J, Chi ZM, Yan KR, Wang XH, Gong F, Li J (2008a) Use of response surface methodology for optimizing process parameters for high inulinase production by the marine yeast Cryptococcus aureus G7a in solid-state fermentation and hydrolysis of inulin. Bioproc Biosyst Eng. doi:https://doi.org/10.1007/s00449-008-0252-2

    Article  PubMed  CAS  Google Scholar 

  • Sheng J, Chi ZM, Gong F, Li J (2008b) Purification and characterization of extracellular inulinase from a marine yeast Cryptococcus aureus G7a and inulin hydrolysis by the purified inulinase. Appl Biochem Biotechnol 144:111–121

    Article  CAS  PubMed  Google Scholar 

  • Silva-Santisteban BOY, Filho FM (2005) Agitation, aeration and shear stress as key factors in inulinase production by Kluyveromyces marxianus. Enzyme Microb Technol 36:717–724

    Article  CAS  Google Scholar 

  • Singh RS, Bhermi HK (2008) Production of extracellular exoinulinase from Kluyveromyces marxianus YS-1 using root tubers of Asparagus officinalis. Biores Technol 99:7418–7423

    Article  CAS  Google Scholar 

  • Singh RS, Sooch BS, Puri M (2007) Optimization of medium and process parameters for the production of inulinase from a newly isolated Kluyveromyces marxianus YS-1. Biores Technol 98:2518–2525

    Article  CAS  Google Scholar 

  • Sirisansaneeyakul S, Worawuthiyanan N, Vanichsriratana W, Srinophakun P, Chisti Y (2008) Production of fructose from inulin using mixed inulinases from Aspergillus niger and Candida guilliermondii. World J Microbiol Biotechnol. doi:https://doi.org/10.1007/s11274-006-9258-6

    Article  CAS  Google Scholar 

  • Szambelan K, Nowak J, Czarnecki Z (2004) Use of Zymomonas mobilis and Saccharomyces cerevisiae mixed with Kluyveromyces fragilis for improved ethanol production from Jerusalem artichoke tubers. Biotechnol Lett 26:845–848

    Article  CAS  PubMed  Google Scholar 

  • Tsujimoto Y, Watanabe A, Nakano K, Watanabe K, Matsui H, Tsuji K, Tsukihara T, Suzuki Y (2003) Gene cloning, expression, and crystallization of a thermostable exo-inulinase from Geobacillus stearothermophilus KP1289. Appl Microbiol Biotechnol 62:180–185

    Article  CAS  PubMed  Google Scholar 

  • Uhm TB, Chae KS, Lee DW, Kim HS, Cassart JP, Vandenhaute J (1998) Cloning and nucleotide sequence of the endoinulinase-encoding gene, inu2 from Aspergillus ficuum. Biotechnol Lett 20:809–812

    Article  CAS  Google Scholar 

  • Wei W, Wang S, Zhu X, Wan W (1999a) Isolation of a mutant of Kluyveromyces sp. Y-85 resistant to catabolite repression. J Biosci Bioeng 87:816–818

    Article  CAS  PubMed  Google Scholar 

  • Wei W, Wan W, Le H, Wang S (1999b) Continuous preparation of fructose syrups from Jerusalem artichoke tuber using immobilized intracellular inulinase from Kluyveromyces sp. Y-85. Proc Biochem 34:643–646

    Article  CAS  Google Scholar 

  • Wei W, Zheng Z, Liu Y, Zhu Z (1998) Optimizing the culture conditions for higher inulinase production Kluyveromyces sp. Y-85 and scaling-up fermentation. J Fermen Bioeng 86:395–399

    Article  CAS  Google Scholar 

  • Wen T, Liu F, Huo K, Li YY (2003) Cloning and analysis of the inulinase gene from Kluyveromyces cicerisporus CBS4857. World J Microbiol Biotechnol 19:423–426

    Article  CAS  Google Scholar 

  • Yu XJ, Guo N, Chi ZM, Gong F, Sheng J, Chi ZM (2008) Inulinase overproduction by a mutant of the marine yeast Pichia guilliermondii using surface response methodology and inulin hydrolysis. Biochem Eng J. doi:https://doi.org/10.1016/j.bej.2008.10.018

    Article  CAS  Google Scholar 

  • Yue LX, Chi ZM, Wang L, Liu J, Madzak C, Li J, Wang XH (2008) Construction of a new plasmid for surface display on cells of Yarrowia lipolytica. J Microbiol Meth 72:116–123

    Article  CAS  Google Scholar 

  • Yun JW, Kim DH, Uhm TB, Song SK (1997) Production of high-content inulo-oligosaccharides from inulin by a purified endoinulinase. Biotechnol Lett 19:935–938

    Article  CAS  Google Scholar 

  • Zhang L, Zhao C, Wang J, Ohta Y, Wang Y (2005) Inhibition of glucose on an exoinulinase from Kluyveromyces marxianus expressed in Pichia pastoris. Proc Biochem 40:1541–1545

    Article  CAS  Google Scholar 

  • Zhang T, Gong F, Chi, Z, Liu GL, Chi, ZM, Sheng J, Li J, Wang XH (2009) Cloning and characterization of the inulinase gene from a marine yeast Pichia guilliermondii and its expression in Pichia pastoris. Antonie van Leeuwenhoek 95:13–22

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Acknowledgements

This work was supported by the Hi-Tech Research and Development Program of China (863; the grant No is 2006AA09Z403) and the National Natural Science Foundation of China (the grant is 30670058).

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Authors and Affiliations

  1. Unesco Chinese Center of Marine Biotechnology, Ocean University of China, Yushan Road, No., 5, Qingdao, China

    Zhenming Chi, Zhe Chi, Tong Zhang, Guanglei Liu & Lixi Yue

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  1. Zhenming Chi
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  2. Zhe Chi
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  3. Tong Zhang
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  4. Guanglei Liu
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  5. Lixi Yue
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Correspondence to Zhenming Chi.

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Chi, Z., Chi, Z., Zhang, T. et al. Inulinase-expressing microorganisms and applications of inulinases. Appl Microbiol Biotechnol 82, 211–220 (2009). https://doi.org/10.1007/s00253-008-1827-1

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  • DOI: https://doi.org/10.1007/s00253-008-1827-1

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