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Microbial enzymatic production and applications of short-chain fructooligosaccharides and inulooligosaccharides: recent advances and current perspectives

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Journal of Industrial Microbiology & Biotechnology

Abstract

The industrial production of short-chain fructooligosaccharides (FOS) and inulooligosaccharides is expanding rapidly due to the pharmaceutical importance of these compounds. These compounds, concisely termed prebiotics, have biofunctional properties and hence health benefits if consumed in recommended dosages. Prebiotics can be produced enzymatically from sucrose elongation or via enzymatic hydrolysis of inulin by exoinulinases and endoinulinases acting alone or synergistically. Exoinulinases cleave the non-reducing β-(2, 1) end of inulin-releasing fructose while endoinulinases act on the internal linkages randomly to release inulotrioses (F3), inulotetraoses (F4) and inulopentaoses (F5) as major products. Fructosyltransferases act by cleaving a sucrose molecule and then transferring the liberated fructose molecule to an acceptor molecule such as sucrose or another oligosaccharide to elongate the short-chain fructooligosaccharide. The FOS produced by the action of fructosyltransferases are 1-kestose (GF2), nystose (GF3) and fructofuranosyl nystose (GF4). The production of high yields of oligosaccharides of specific chain length from simple raw materials such as inulin and sucrose is a technical challenge. This paper critically explores recent research trends in the production and application of short-chain oligosaccharides. Inulin and enzyme sources for the production of prebiotics are discussed. The mechanism of FOS chain elongation and also the health benefits associated with prebiotics consumption are discussed in detail.

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References

  1. Alles MS, Hartemink R, Meyboom S, Harryvan JL, Van Laere KMJ, Nagengast FM, Hautvast JGAJ (1999) Effect of transgalactooligosaccharides on the composition of the human intestinal microflora and on putative risk markers for colon cancer. Am J Clinl Nutr 69:980–991

    CAS  Google Scholar 

  2. Alloui MN, Szczurek W, Swiatkiewicz S (2013) The usefulness of prebiotics and probiotics in modern poultry nutrition: a review. Ann Anim Sci 13(1):17–32

    Google Scholar 

  3. Altunbaş C, Uygun M, Uygun DA, Akgöl S, Denizli A (2013) Immobilization of inulinase on concanavalin A-attached super macroporous cryogel for production of high-fructose syrup. Appl Biochem Biotech 170:1909–1921

    Google Scholar 

  4. Azis BH, Chin B, Deacon MP, Harding SE, Pavlov GM (1999) Size and shape of inulin dimethyl sulphoxide solution. Carbohyd Polym 38:231–234

    CAS  Google Scholar 

  5. Barthomeuf C, Grizard D, Teulade JC (1997) Assay and structural determination of fructooligosaccharides synthesized by an enzymatic system from Penicillium rugulosum. Biotechnol Tech 11:845–848

    CAS  Google Scholar 

  6. Biedrzyka E, Bielecka M (2004) Prebiotic effectiveness of fructans of different degrees of polymerization. Trends Food Sci Tech 15:170–175

    Google Scholar 

  7. Brownawell AM, Caers W, Gibson GR, Kendall CWC, Lewis KD, Ringel Y, Slavin JL (2012) Prebiotics and the health benefits of fiber: current regulatory status, future research, and goals. J Nutr 142:962–974

    CAS  PubMed  Google Scholar 

  8. Bruins ME, Strubel M, van Lieshout JFT, Janssen AEM, Boom RM (2003) Oligosaccharide synthesis by the hyperthermostable β-glucosidase from Pyrococcus furiosus: kinetics and modeling. Enzyme Microb Tech 33:3–11

    CAS  Google Scholar 

  9. Buddington RK, Kelly-Quagliana K, Buddington KK, Kimura Y (2002) Non-digestible oligosaccharides and defence functions: lessons learned from animal models. Brit J Nutr 87:S231–S239

    CAS  PubMed  Google Scholar 

  10. Bunesova V, Vlkova E, Rada V, Knazovicka V, Rockova S, Gelgerova M, Bozik M (2012) Growth of infant fecal bacteria on commercial prebiotics. Folia Microbiol 57:273–275

    CAS  Google Scholar 

  11. Burr G, Hume M, Ricke S, Nisbet D, Gatlin D III (2010) In vitro and in vivo evaluation of the prebiotics GroBiotic®-A, inulin, mannanoligosaccharide, and galactooligosaccharide on the digestive microbiota and performance of hybrid striped bass (Morone chrysops × Morone saxatilis). Microb Ecol 59:187–198

    CAS  PubMed  Google Scholar 

  12. Cairns AJ (1993) Evidence for de novo synthesis of fructan by enzymes from higher plants, a reappraisal of the SST/FFT model. New Phytol 123:15–24

    CAS  Google Scholar 

  13. Cairns AJ (1995) Effects of enzyme concentration on oligofructan synthesis from sucrose. Phytochemistry 40(3):705–708

    CAS  Google Scholar 

  14. Callaway TR, Edrington TS, Anderson RC, Harvey RB, Genovese KJ, Kennedy CN, Venn DW, Nisbet DJ (2008) Probiotics, prebiotics and competitive exclusion for prophylaxis against bacterial disease. Anim Health Res Rev 9(2):217–225

    CAS  PubMed  Google Scholar 

  15. Catana R, Eloy M, Rocha JR, Ferreira BS, Cabral J, Fernandes P (2007) Stability evaluation of an immobilized enzyme system for inulin hydrolysis. Anal Biochem 101:260–266

    CAS  Google Scholar 

  16. Cerantola S, Kervarec N, Pichon R, Magne C, Bessiere MA, Deslandes E (2004) NMR characterization of inulin-type fructooligosaccharides as the major water soluble carbohydrates from Matricaria maritime (L.). Carbohyd Res 339:2445–2449

    CAS  Google Scholar 

  17. Chauhan SV, Chorawala MR (2012) Probiotics, prebiotics and synbiotics. Int J Pharm Sci Res 3(3):711–726

    CAS  Google Scholar 

  18. Cherbut C (2002) Inulin and oligofructose in the dietary fibre concept. Brit J Nutr 87:S159–S162

    CAS  PubMed  Google Scholar 

  19. Corradini C, Bianchi F, Matteuzzi D, Amoreti A, Rossi M, Zanoni S (2004) High-performance anion-exchange chromatography coupled with pulsed amperometric detection and capillary zone electrophoresis with indirect ultra violet detection as powerful tools to evaluate prebiotic properties of fructooligosaccharides and inulin. J Chromatogr A 1054:165–173

    CAS  PubMed  Google Scholar 

  20. Crittenden RJ, Playne MJ (2002) Purification of food grade oligosaccharides using immobilised cells of Zymomonas mobilis. Appl Microbiol Biot 58:297–302

    CAS  Google Scholar 

  21. Crittenden RG, Playne MJ (1996) Production, properties and applications of food-grade oligosaccharides. Trends Food Sci Tech 7:353–361

    CAS  Google Scholar 

  22. Cummings JH, Macfarlane GT (2002) Gastrointestinal effects of prebiotics. Brit J Nutr 87(2):S145–S151

    CAS  PubMed  Google Scholar 

  23. De Leenher L, Hoebregs H (1994) Progress in the elucidation of the composition of chicory inulin. Starch 46:193–196

    Google Scholar 

  24. De Sousa VMC, dos Santos EF, Sgarbieri VC (2011) The importance of prebiotics in functional foods and clinical practice. Food Nutr Sci 2:133–144

    Google Scholar 

  25. Delzenne NM, Daubioul C, Neyrinck A, Lasa M, Taper HS (2002) Inulin and oligofructose modulate lipid metabolism in animals: review of biochemical events and future prospects. Brit J Nutr 87:S255–S259

    CAS  PubMed  Google Scholar 

  26. Diaz EG, Catana R, Ferreira BS, Luque S, Fernandes P, Cabral JMS (2006) Towards the development of a membrane reactor for enzymatic inulin hydrolysis. J Membrane Sci 273:152–158

    CAS  Google Scholar 

  27. Durieux A, Fougnies C, Jacobs H, Simon JP (2001) Metabolism of chicory fructooligosaccharides by bifidobacteria. Biotechnol Lett 23:1523–1527

    CAS  Google Scholar 

  28. Duus J, Gotfredsen CH, Bock K (2000) Carbohydrate structural determination by NMR spectroscopy: modern methods and limitations. Chem Rev 100:4589–4614

    CAS  PubMed  Google Scholar 

  29. Edelman J, Jefford TG (1968) The mechanism of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytol 67:517–531

    CAS  Google Scholar 

  30. Everard A, Lazarevic V, Derrien M, Girard M, Muccioli GM, Neyrinck AM, Possemiers S, Van Holle A, Francois P, de Vos WM, Delzenne NM, Schrenzel J, Cani PD (2011) Responses of gut microbiota and glucose and lipid metabolism to prebiotics in genetic obese and diet-induced leptin-resistant mice. Diabetes 60(11):2775–2786

    CAS  PubMed Central  PubMed  Google Scholar 

  31. Flamm G, Glinsmann W, Kritchevsky D, Prosky L, Roberfroid M (2001) Inulin and oligofructose as dietary fibre: a review of the evidence. CRC Cr Rev Food Sci 41:353–362

    CAS  Google Scholar 

  32. Flickinger EA, Loo JV, Fahey GC (2003) Nutritional responses to the presence of inulin and oligofructose in the diets of domesticated animals. A review. CRC Cr Rev Food Sci 43:19–60

    CAS  Google Scholar 

  33. French AD (1988) Accessible conformations of the β-d-(2 → 1)-and-(2 → 6)-linked d-fructans inulin and levan. Carbohyd Res 176:17–29

    CAS  Google Scholar 

  34. Freitas KC, Amancio OMS, de Morais MB (2012) High-performance inulin and oligofructose prebiotics increase the intestinal absorption of iron in rats with iron deficiency anaemia during the growth phase. Brit J Nutr 108:1008–1016

    CAS  Google Scholar 

  35. Fujita K, Kuwahara N, Tanimoto T, Koizumi K, Iizuka M, Minamiura N (1994) Chemical structures of hetero-oligosaccharides produced by Arthrobacter sp. K-1 -fructofuranosidase. Biosci Biotech Bioch 58:239–243

    CAS  Google Scholar 

  36. Ghazi I, Fernandez-Arrojo L, de Segura Gomez A, Alcalde M, Plou FJ, Ballesteros A (2006) Beet sugar and molasses as lo-cost feedstock for the enzymatic production of fructooligosaccharides. J Agric Food Chem 54:2964–2968

    CAS  PubMed  Google Scholar 

  37. Giacco R, Clemente G, Luongo D, Lasorella G, Fiume I, Brouns F, Bornet F, Patti L, Cipriano P, Rivellese AA, Riccardi G (2004) Effects of short-chain fructooligosaccharides on glucose and lipid metabolism in mild hypercholesterolaemic individuals. Clin Nutr 23:331–340

    CAS  PubMed  Google Scholar 

  38. Gibson GR, Fuller R (2000) Aspects of in vitro and in vivo research approaches directed towards identifying probiotics and prebiotics for human use. J Nutr 130(2S):391S–395S

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  40. Gonta S, Utinans M, Neilands O, Vina I (2004) Computational analysis of native and modified oligofructosides. J Mol Struc-Theochem 710:61–64

    CAS  Google Scholar 

  41. Goulas A, Tzortzis G, Gibson GR (2007) Development of a process for the production and purification of α- and β-galactooligosaccharides from Bifidobacterium bifidum NCIMB 41171. Int Dairy J 17:648–656

    CAS  Google Scholar 

  42. Goulas AK, Kapasakalidis PG, Sinclair HR, Rastall RA, Grandison AS (2002) Purification of oligosaccharides by nanofiltration. J Membrane Sci 209:321–335

    CAS  Google Scholar 

  43. Guignard C, Jouve L, Bogeat-Triboulot MB, Dreyer E, Hausman JF, Hoffmann L (2005) Analysis of carbohydrates in plants by high-performance anion-exchange chromatography coupled with electrospray mass spectrometry. J Chromatog A 1085:137–142

    CAS  Google Scholar 

  44. Hebette CLM, Delcour JA, Koch MHJ, Booten K, Kleppinger R, Mischenko N, Reynaers H (1998) Complex melting of semi-crystalline chicory (Cichorium intybus L.) root inulin. Carbohyd Res 310:65–75

    CAS  Google Scholar 

  45. Heyer AG, Lloyd JR, Kossmann J (1999) Production of modified polymeric carbohydrates. Curr Opin Biotech 10:169–174

    CAS  PubMed  Google Scholar 

  46. Hicke HG, Ulbricht M, Becker M, Radosta S, Heyer AG (1999) Novel enzyme-membrane reactor for polysaccharide synthesis. J Membrane Sci 161:239–245

    CAS  Google Scholar 

  47. Hicks PD, Hawthorne KH, Berseth CL, Marunycz JD, Heubi J, Abrams SA (2012) Total calcium absorption is similar from infant formulas with and without prebiotics and exceeds that in human milk-fed infants. BMC Pediatr 12(118):2–6

    Google Scholar 

  48. Huebner J, Wehling RL, Hutkins RW (2007) Functional activity of commercial prebiotics. Int Dairy J 17:770–775

    CAS  Google Scholar 

  49. Ishwarya SP, Prabhasankar P (2013) Fructooligosaccharide: retention during baking and its influence on biscuit quality. Food Biosci 4:68–80

    Google Scholar 

  50. Itaya NM, Asega AF, Carvalho MAM, Figueiredo-Ribeiro RL (2007) Hydrolase and fructosyltransferase activities implicated in the accumulation of different chain size fructans in three Asteracea species. Plant Physiol Bioch 45:647–656

    CAS  Google Scholar 

  51. Janardhana V, Broadway MM, Bruce MP, Lowenthal JW, Geier MS, Hughes RJ, Bean AGD (2009) Prebiotics modulate immune responses in the gut-associated lymphoid tissue of chickens1-3. J Nutr 139(7):1404–1409

    CAS  PubMed  Google Scholar 

  52. Jing W, Zhengyu J, Bo J, Xueming X (2003) Separation and identification of exo- and endoinulinase from Aspergillus ficuum. Curr Microbiol 47:109–112

    PubMed  Google Scholar 

  53. Jing W, Zhengyu J, Bo J, Augustine A (2003) Production and separation of exo- and endoinulinase from Aspergillus ficcum. Process Biochem 39:5–11

    Google Scholar 

  54. Jung KH, Yun JW, Kang KR, Lim JY, Lee JH (1989) Mathematical model for enzymatic production of fructo-oligosaccharides from sucrose. Enzyme Microb Tech 11:491–494

    CAS  Google Scholar 

  55. Kalil SJ, Suzan R, Maugeri F, Rodrigues MI (2001) Optimisation of inulinase production by Kluyveromyces marxianus using factorial design. Appl Biochem Biotech 94:257–264

    CAS  Google Scholar 

  56. Kim JH, An HJ, Garrido D, German JB, Lebrilla CB (2013) Proteomic analysis of Bifidobacterium longum subsp. infantis reveals the metabolic insight on consumption of prebiotics and host glycans. PLoS ONE 8(2):e57535. doi:10.1371/journal.pone.0057535

    CAS  PubMed Central  PubMed  Google Scholar 

  57. Koops AJ, Jonker HH (1994) Purification and characterisation of the enzymes of fructan biosynthesis in tubers of Helianthus tuberosus Colombia. I. Fructan 1-fructosyltransferase. J Exp Bot 45:1623–1631

    CAS  Google Scholar 

  58. Kuhn GO, Rosa CD, Silva MF, Treichel H, Oliveira D, Oliveira JV (2013) Synthesis of fructooligosaccharides from Aspergillus niger commercial inulinase immobilized in Montmorillonite pretreated in pressurized propane and LPG. Appl Biochem Biotech 169:750–760

    Google Scholar 

  59. Kuroiwa T, Ichikawa S, Hiruta O, Sato S, Mukataka S (2002) Factors affecting the composition of oligosaccharides produced in chitosan hydrolysis using immobilized chitosanases. Biotechnol Progr 18:969–974

    CAS  Google Scholar 

  60. Leiti JTC, Martinelli P, Murr FEX, Jin K (2004) Study of the inulin concentration by physical methods. In: Proceedings of the 14th International Drying Symposium (IDS2004) Sao Paulo, Brazil, 22-25 Aug 2004 B, pp 868–875

  61. Lewis DH (1993) Nomenclature and diagrammatic representation of oligomeric fructans a paper for discussion. New Phytol 124:583–594

    CAS  Google Scholar 

  62. Lenoir-Wijnkoop L, van Aalderen WMC, Boehm G, Klaassen D, Sprikkelman AB, Nuijten MJC (2012) Cost-effectiveness model for a specific mixture of prebiotics in The Netherlands. Eur J Health Econ 13:101–110

    CAS  PubMed  Google Scholar 

  63. Lingyun W, Jianhua W, Xiaodong Z, Da T, Yalin Y, Chenggang C, Tianhua F, Fan Z (2007) Studies on the extracting technical conditions of inulin from Jerusalem artichoke tubers. J Food Eng 79:1087–1093

    Google Scholar 

  64. Loo JV, Coussement P, Leenheer L, de Hoebregs H, Smits G (1995) On the presence of inulin and oligofructose as natural ingredients in the western diets. Crit Rev Food Sci 35:525–552

    Google Scholar 

  65. López-Molina D, Navarro-Martínez MD, Melgarejo FR, Hiner ANP, Chazarra S, Rodríguez-López JN (2005) Molecular properties and prebiotic effect of inulin obtained from artichoke (Cyanara scolymus L.). Phytochemistry 66:1476–1484

    PubMed  Google Scholar 

  66. Luo J, Yperselle MV, Rizkalla SW, Rossi F, Bornet FRJ, Slama G (2000) Chronic consumption of short chain fructooligosaccharides does not affect basal hepatic glucose production or insulin resistance in type 2 diabetics. J Nutr 130:1572–1577

    CAS  PubMed  Google Scholar 

  67. Luscher M, Erdin C, Sprenger N, Hochstrasser U, Boller T, Wiemken A (1996) Inulin hydrolysis by a combination of purified fructosyltransferases from tubers of Helianthus tuberosus. FEBS Lett 383:39–42

    Google Scholar 

  68. Ma AYM, Ooraikul B (1986) Optimisation of enzymatic hydrolysis of canola meal with response surface methodology. J Food Proc Preserv 10:99–113

    Google Scholar 

  69. Mesanetz S, Preibinger W, Meyer HHD, Pfaffl MW (2011) Effects of the prebiotics inulin and lactulose on intestinal immunology and hematology of preruminant calves. Animal 5(7):1099–1106

    Google Scholar 

  70. Messier C, Whately K, Liang J, Du L, Puissant D (2007) The effects of a high-fat, high-fructose, and combination diet on learning, weight, and glucose regulation in C57BL/6 mice. Behav Brain Res 178:139–145

    CAS  PubMed  Google Scholar 

  71. Mislovicova D, Michalkova E, Vikartovska A (2007) Immobilized glucose oxidase on different supports for biotransformation removal of glucose from oligosaccharide mixtures. Process Biochem 42:704–709

    CAS  Google Scholar 

  72. Mitsuoka T (1990) Bifidobacteria and their role in human health. J Ind Microbiol Biot 6:263–267

    Google Scholar 

  73. Modler HW (1994) Bifidogenic factors-sources, metabolism and applications. Int Dairy J 4:383–407

    Google Scholar 

  74. Mugambi MN, Musekiwa A, Lombard M, Young T, Blaauw R (2012) Synbiotics, probiotics or prebiotics in infant formula for full term infants: a systematic review. Nutr J 11(81):1–32

    Google Scholar 

  75. Mutanda T, Wilhelmi B, Whiteley CG (2008) Response surface methodology: synthesis of Inulo-oligosaccharides with an Endoinulinase from Aspergillus niger. Enzyme Microb Tech 43:362–368

    CAS  Google Scholar 

  76. Nagem RAP, Rojas AL, Golubev AM, Korneeva AS, 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

    CAS  PubMed  Google Scholar 

  77. 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 Ferment Bioeng 80:164–169

    CAS  Google Scholar 

  78. Nemukula A, Mutanda T, Wilhelmi B, Whiteley CG (2009) Response surface methodology: synthesis of short chain Fructooligosaccharides with a fructosyltransferase from Aspergillus aculeatus. Bioresource Technol 100:2040–2045

    CAS  Google Scholar 

  79. Nguyen QD, Rezessy-Szabo JM, Czukor B, Hoschke A (2011) Continuous production of oligofructose syrup from Jerusalem artichoke juice by immobilized endo-inulinase. Process Biochem 46:298–303

    CAS  Google Scholar 

  80. Niness KR (1999) Inulin and oligofructose: what are they? J Nutr 129:1402S–1406S

    CAS  PubMed  Google Scholar 

  81. Ohta K, Suetsugu N, Nakamura T (2002) Purification and properties of an extracellular inulinase from Rhizopus sp. strain TN-96. J Biosci Bioeng 94:78–80

    CAS  PubMed  Google Scholar 

  82. Pandey A, Soccol CR, Selvakumar P, Soccol VT, Krieger N, Fontana JD (1999) Recent developments in microbial inulinases. Appl Biochem Biotech 81:35–52

    CAS  Google Scholar 

  83. Park JP, Bae JT, Yun JW (1999) Critical effect of ammonium ions on the enzymatic reaction of a novel transfructosylating enzyme for fructooligosaccharide production from sucrose. Biotechnol Lett 21:987–990

    CAS  Google Scholar 

  84. Paseephol T, Small D, Sherkat F (2007) Process optimization for fractionating Jerusalem artichoke fructans with ethanol using response surface methodology. Food Chem 104:73–80

    CAS  Google Scholar 

  85. Patra AK (2011) Responses of feeding prebiotics on nutrient digestibility, faecal microbiota composition and short-chain fatty acid concentrations in dogs: a meta-analysis. Animal 5(11):1743–1750

    CAS  PubMed  Google Scholar 

  86. Pool-Zobel B, van Loo J, Rowland I, Roberfroid MB (2002) Experimental evidences on the potential of prebiotic fructans to reduce the risk of colon cancer. Brit J Nutr 87:S273–S281

    CAS  PubMed  Google Scholar 

  87. Prapulla SG, Subhaprada V, Karanth NG (2000) Microbial production of oligosaccharides: a review. Adv Appl Microbiol 47:243–299

    Google Scholar 

  88. Risso FVA, Mazutti MA, Treichel H, Costa F, Maugeri F, Rodrigues MI (2010) Synthesis of fructooligosaccharides from sucrose in aqueous & aqueous-organic systems using free inulinase from Kluyveromyces marxianus ATCC 16045. Ind Biotechnol 6(5):288–294

    CAS  Google Scholar 

  89. Roberfroid MB, Van Loo JAE, Gibson GR (1998) The bifidogenic nature of chicory inulin and its hydrolysis products. J Nutr 128:11–19

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  91. Rycroft CE, Jones MR, Gibson GR, Rastall RA (2001) A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. J Appl Microbiol 91:878–887

    CAS  PubMed  Google Scholar 

  92. Sangeetha PT, Ramesh MN, Prapulla SG (2005) Recent trends in the production, analysis and application of Fructooligosaccharides. Trends Food Sci Tech 16:442–457

    CAS  Google Scholar 

  93. Sanz ML, Martinez-Castro I (2007) Recent developments in sample preparation for chromatographic analysis of carbohydrates. J Chromatogr A 1153:74–89

    CAS  PubMed  Google Scholar 

  94. Scholz-Ahrens KE, Schrezenmeir J (2002) Inulin, oligofructose and mineral metabolism: experimental data and mechanism. Brit J Nutr 87:S179–S186

    CAS  PubMed  Google Scholar 

  95. Seeberger PH, Werz DB (2007) Synthesis and medical applications of oligosaccharides. Nature 446:1046–1051

    CAS  PubMed  Google Scholar 

  96. Sharma AD, Kainth S, Gill PK (2006) Inulinase production using garlic (Allium sativum) powder as a potential substrate in Streptomyces sp. J Food Eng 77:486–491

    CAS  Google Scholar 

  97. Sharma AD, Gill PK (2007) Purification and characterization of heat stable exo-inulinase from Streptomyces sp. J Food Eng 79:1172–1178

    CAS  Google Scholar 

  98. Sharma S, Agarwal N, Verma P (2012) Miraculous health benefits of prebiotics. IJPSR 3(6):1544–1553

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  100. Sheu DC, Lio PJ, Chen ST, Lin CT, Duan KJ (2001) Production of fructooligosaccharides in high yield using a mixed enzyme system of β-fructosidase and glucose oxidase. Biotechnol Lett 23:1499–1503

    CAS  Google Scholar 

  101. Simmen U, Obenland D, Boller T, Wienken A (1993) Fructan synthesis in excised barley leaves. Identification of two sucrose–sucrose fructosyltransferases induced by light and their separation from constitutive invertases. Plant Physiol 101:459–468

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Sjoman E, Manttari M, Nystrom M, Koivikko H, Heikkila H (2007) Separation of xylose from glucose by nanofiltration from concentrated monosaccharide solutions. J Membrane Sci 292:106–115

    Google Scholar 

  103. Steinberg D, Rozen R, Bromshteym M, Zaks B, Gedalia I, Bachrach G (2002) Regulation of fructosyltransferase activity by carbohydrates, in solution and immobilized on hydroxyapatite surfaces. Carbohyd Res 337:701–710

    CAS  Google Scholar 

  104. Szkaradkiewicz AK, Karpinski TM (2013) Probiotics and prebiotics. J Biol Earth Sci 3(1):M42–M47

    Google Scholar 

  105. Tanriseven A, Aslan Y (2005) Immobilization of Pectinex Ultra SP-L to produce fructooligosaccharides. Enzyme Microb Tech 36:550–554

    CAS  Google Scholar 

  106. Tanriseven A, Gokmen F (1999) Novel method for the production of a mixture containing fructooligosaccharides and isomaltooligosaccharides. Biotechnol Tech 13:207–210

    CAS  Google Scholar 

  107. Taper HS, Roberfroid MB (2002) Inulin/oligofructose and anticancer therapy. Brit J Nutr 87:S283–S286

    CAS  PubMed  Google Scholar 

  108. To´fano J, Toneli CL, Murr FEX, Martinelli P, Fabbro IM, Park KJ (2007) Optimisation of a physical concentration process for inulin. J Food Eng 80:832–838

    Google Scholar 

  109. Tomotani EJ, Vitolo M (2007) Production of high-fructose syrup using immobilized invertase in a membrane reactor. J Food Eng 80:662–667

    CAS  Google Scholar 

  110. Vandamme EJ, Derycke DG (1983) Microbial inulinases: fermentation process, properties and applications. Adv Appl Microbiol 29:139–176

    CAS  PubMed  Google Scholar 

  111. Van den Burg B (2003) Extremophiles as source for novel enzymes. Curr Opin Microbiol 6:213–218

    PubMed  Google Scholar 

  112. Van den Ende W, Van Laere A (1996) De novo synthesis of fructans from sucrose in vitro by a combination of two purified enzymes (sucrose: sucrose 1-fructosyl transferase and fructan: fructan 1-fructosyl transferase) from chicory roots (Cichorium intybus L.). Planta 200:335–342

    Google Scholar 

  113. Van den Ende W, Michiels A, Van Wonterghem D, Vergauwen R, Van Laere A (2000) Cloning, developmental, and Tissue-specific expression of sucrose: sucrose 1-fructosyl transferase from Taraxacum officinale. Fructan localization in roots. Plant Physiol 123:71–79

    PubMed Central  PubMed  Google Scholar 

  114. Van den Ende W, Clerens S, Vergauwen R, Van Riet L, Van Laere A, Yoshida M, Kawakami A (2003) Fructan 1-exohydrolase. Beta-(2, 1)-trimmers during graminan biosynthesis in stems of wheat? Purification, characterisation, mass mapping, and cloning of two fructan 1-exohydrolase isoforms. Plant Physiol 131:621–631

    PubMed Central  Google Scholar 

  115. Van den Ende W, De Coninck B, Van Laere A (2004) Plant fructanexohydrolase: a role in signaling and defense? Trends Plant Sci 9(11):523–528

    PubMed  Google Scholar 

  116. Van Der Heijden AM, Van Hoek P, Kaliterna J, Van Dijken JP, Van Rantwijk F, Pronk JT (1999) Use of the yeast Hansenula polymorpha (Pichia angusta) to remove contaminating sugars from ethyl/3-d-fructofuranoside produced during sucrose ethanolysis catalysed by invertase. J Biosci Bioeng 87(1):82–86

    PubMed  Google Scholar 

  117. Van Laere KMJ, Abee T, Schools HA, Beldman G, Voragen AGJ (2000) Characterization of a novel β-galactosidase from Bifidobacterium adolescentis DSM 20083 active towards transgalactooligosaccharides. Appl Environ Microb 66(4):1379–1384

    Google Scholar 

  118. Van Loo J, Coussement P, De Leeheer L, Hoebregs H, Smits G (1995) On the presence of inulin and oligofructose as natural ingredients in the western diet. CRC Cr Rev Food Sci 35:525–552

    Google Scholar 

  119. Van Stuijvenberg M, Eisses AM, Gruber C, Mosca F, Arslanoglu S, Chirico G, Braegger CP, Riedler J, Boehm G, Sauer PJJ (2011) Do prebiotics reduce the number of fever episodes in healthy children in their first year of life: a randomised controlled trial. Brit J Nutr 106:1740–1748

    PubMed  Google Scholar 

  120. Van Waes C, Baert J, Carlier L, Van Bockstaele E (1998) A rapid determination of the total sugar content and the average inulin chain length in roots of chicory (Cichorium intybus L.). J Sci Food Agr 76:107–110

    Google Scholar 

  121. Vazquez MJ, Alonso JL, Dominguez H, Parajo JC (2000) Xylooligosaccharides: manufacture and applications. Trends Food Sci Tech 87:387–393

    Google Scholar 

  122. Villegas B, Costell E (2007) Flow behaviour of inulin–milk beverages. Influence of inulin average chain length and of milk fat content. Int Dairy J 17:776–781

    CAS  Google Scholar 

  123. Wang J, Sporns P, Low NH (1999) Analysis of food oligosaccharides using MALDI-MS: quantification of fructooligosaccharides. J Agr Food Chem 47:1549–1557

    CAS  Google Scholar 

  124. Xiong C, Jinhua W, Dongsheng L (2007) Optimization of solid-state medium for the production of inulinase by Kluyveromyces S120 using response surface methodology. Biochem Eng J 34:179–184

    CAS  Google Scholar 

  125. Yoon EJ, Yoo SH, Chac J, Lee HG (2004) Effect of levan’s branching structure on antitumor activity. Int J Biol Macromol 34:191–194

    CAS  PubMed  Google Scholar 

  126. Yoon SH, Mukerjea R, Robyt JF (2003) Specificity of yeast (Saccharomyces cerevisiae) in removing carbohydrates by fermentation. Carbohyd Res 338:1127–1132

    CAS  Google Scholar 

  127. Yun JW (1996) Fructooligosaccharides occurrence, preparation, and application. Enzyme Microb Tech 19(2):107–117

    CAS  Google Scholar 

  128. Yun JW, Kim DH, Uhm TB, Song SK (1997) Production of high content inulo-oligosaccharides from inulin by a purified endoinulinase. Biotechnol Lett 19(9):935–938

    CAS  Google Scholar 

  129. Yun JW, Park JP, Song JP, Lee CY, Kim JH, Song SK (2000) Continuous production of inulo-oligosaccharides from chicory juice by immobilised endoinulinase. Bioproc Biosyst Eng 22:189–194

    CAS  Google Scholar 

  130. Zhengyu J, Jing W, Bo J, Xueming X (2005) Production of inulooligosaccharides by endoinulinases from Aspergillus ficuum. Food Res Int 38:301–308

    Google Scholar 

  131. He M, Wu D, Wu J, Chen J (2014) Enhanced expression of endoinulinase from Aspergillus niger by codon optimization in Pichia pastoris and its application in inulooligosaccharides production. J Ind Microbiol Biotechnol 41:105–114

    CAS  PubMed  Google Scholar 

  132. Huitron C, Perez R, Gutierrez L, Lappe P, Petrosyan P, Villegas J, Aguilar C, Rocha-Zavalata L, Blancas A (2013) Bioconversion of Agave tequilana fructans by exo-inulinase from indigenous Aspergillus niger CH-A-2010 enhances ethanol production from raw Agave tequilana juice. J Ind Microbiol Biotechnol 40:123–132

    CAS  PubMed  Google Scholar 

  133. Olivares-Illana V, Wacher-Rodarte C, Le Borgne S, Lopez-Munguia A (2013) Characterisation of a cell associated inulosucrase from a novel source: a Leuconostoc citreum strain isolated from Pozol, a fermented corn beverage of Mayan origin. J Ind Microbiol Biotechnol 28:112–117

    Google Scholar 

  134. Gualtieri KA, Guembarovski RL, Oda JMM, Fiori-Lopes L, Carneiro NK, de Castro VD, Neto JS, Watanabe MAE (2013) Inulin: therapeutic potential, prebiotic properties and immunological aspects. Food Agric Immunol 24(1):21–31

    CAS  Google Scholar 

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Acknowledgments

All authors have agreed to submit this manuscript to the “Journal of Industrial Microbiology and Biotechnology”. The authors declare that they have no conflict of interest. The authors would like to acknowledge The National Research Foundation—Technology and Human Resources for Industry Programme (NRF-THRIP), Rhodes University and the University of KwaZulu Natal for funding this project.

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Mutanda, T., Mokoena, M.P., Olaniran, A.O. et al. Microbial enzymatic production and applications of short-chain fructooligosaccharides and inulooligosaccharides: recent advances and current perspectives. J Ind Microbiol Biotechnol 41, 893–906 (2014). https://doi.org/10.1007/s10295-014-1452-1

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