Skip to main content

Advertisement

Log in

Prebiotic Oligosaccharides: Special Focus on Fructooligosaccharides, Its Biosynthesis and Bioactivity

  • Published:
Applied Biochemistry and Biotechnology Aims and scope Submit manuscript

Abstract

The bacterial groups in the gut ecosystem play key role in the maintenance of host’s metabolic and structural functionality. The gut microbiota enhances digestion processing, helps in digestion of complex substances, synthesizes beneficial bioactive compounds, enhances bioavailability of minerals, impedes growth of pathogenic microbes, and prevents various diseases. It is, therefore, desirable to have an adequate intake of prebiotic biomolecules, which promote favorable modulation of intestinal microflora. Prebiotics are non-digestible and chemically stable structures that significantly enhance growth and functionality of gut microflora. The non-digestible carbohydrate, mainly oligosaccharides, covers a major part of total available prebiotics as dietary additives. The review describes the types of prebiotic low molecular weight carbohydrates, i.e., oligosaccharides, their structure, biosynthesis, functionality, and applications, with a special focus given to fructooligosaccharides (FOSs). The review provides an update on enzymes executing hydrolytic and fructosyltransferase activities producing prebiotic FOS biomolecules, and future perspectives.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Raman, M., Ambalam, P., & Doble, M. (2016). Bioactive carbohydrate: prebiotics and colorectal cancer. In probiotics and bioactive carbohydrates in colon cancer management. Springer India, 57–82.

  2. Hutkins, R. W., Krumbeck, J. A., Bindels, L. B., Cani, P. D., Fahey, G., Goh, Y. J., Hamaker, B., Martens, E. C., Mills, D. A., Rastal, R. A., & Vaughan, E. (2016). Prebiotics: why definitions matter. Current Opinion in Biotechnology, 37, 1–7.

    Article  CAS  Google Scholar 

  3. Younis, K., Ahmad, S., & Jahan, K. (2015). Health benefits and application of prebiotics in foods. Journal of Food Processing and Technology, 6(433), 2.

    Google Scholar 

  4. Rastall, R. A. (2010). Functional oligosaccharides: application and manufacture. Annual Review of Food Science and Technology, 1, 305–339.

    Article  CAS  Google Scholar 

  5. Gibson, G. R., & Roberfroid, M. B. (1995). Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. The Journal of Nutrition, 125(6), 1401.

    CAS  Google Scholar 

  6. Vandenplas, Y., Zakharova, I., & Dmitrieva, Y. (2015). Oligosaccharides in infant formula: more evidence to validate the role of prebiotics. British Journal of Nutrition, 113(09), 1339–1344.

    Article  CAS  Google Scholar 

  7. Bird, A., Conlon, M., Christophersen, C., & Topping, D. (2010). Resistant starch, large bowel fermentation and a broader perspective of prebiotics and probiotics. Beneficial Microbes, 1(4), 423–431.

    Article  CAS  Google Scholar 

  8. Puertollano, E., Kolida, S., & Yaqoob, P. (2014). Biological significance of short-chain fatty acid metabolism by the intestinal microbiome. Current Opinion in Clinical Nutrition & Metabolic Care, 17(2), 139–144.

    Article  CAS  Google Scholar 

  9. Ríos-Covián, D., Ruas-Madiedo, P., Margolles, A., Gueimonde, M., & de los Reyes-Gavilán, C.G. & Salazar, N. (2016). Intestinal short chain fatty acids and their link with diet and human health. Frontiers in Microbiology, 7. https://doi.org/10.3389/fmicb.2016.00185.

  10. Itaya, N. M., Asega, A. F., Carvalho, M. A. M., & Rita de Cássia, L. (2007). Hydrolase and fructosyltransferase activities implicated in the accumulation of different chain size fructans in three Asteraceae species. Plant Physiology and Biochemistry, 45(9), 647–656.

    Article  CAS  Google Scholar 

  11. Sangeetha, P. T., Ramesh, M. N., & Prapulla, S. G. (2005). Recent trends in the microbial production, analysis and application of fructooligosaccharides. Trends in Food Science & Technology, 16(10), 442–457.

    Article  CAS  Google Scholar 

  12. Voragen, A. G. (1998). Technological aspects of functional food-related carbohydrates. Trends in Food Science & Technology, 9(8), 328–335.

    Article  CAS  Google Scholar 

  13. Prakash, M. D. (1984). Occurrence of glycoprotein glycosidases in mature seeds of mung bean (Vigna radiata). Phytochemistry, 23(2), 257–260.

    Article  Google Scholar 

  14. Moure, A., Gullón, P., Domínguez, H., & Parajó, J. C. (2006). Advances in the manufacture, purification and applications of xylooligosaccharides as food additives and nutraceuticals. Process Biochemistry, 41(9), 1913–1923.

    Article  CAS  Google Scholar 

  15. Intanon, M., Arreola, S. L., Pham, N. H., Kneifel, W., Haltrich, D., & Nguyen, T. H. (2014). Nature and biosynthesis of galactooligosaccharides related to oligosaccharides in human breast milk. FEMS Microbiology Letters, 353(2), 89–97.

    Article  CAS  Google Scholar 

  16. Lina, B. A. R., Jonker, D., & Kozianowski, G. (2002). Isomaltulose (Palatinose®): A review of biological and toxicological studies. Food and Chemical Toxicology, 40(10), 1375–1381.

    Article  CAS  Google Scholar 

  17. Holck, J., Hjernø, K., Lorentzen, A., Vigsnæs, L. K., Hemmingsen, L., Licht, T. R., Mikkelsen, J. D., & Meyer, A. S. (2011). Tailored enzymatic production of oligosaccharides from sugar beet pectin and evidence of differential effects of a single DP chain length difference on human faecal microbiota composition after in vitro fermentation. Process Biochemistry, 46(5), 1039–1049.

    Article  CAS  Google Scholar 

  18. Kwon, H. J., Jeon, S. J., You, D. J., Kim, K. H., Jeong, Y. K., Kim, Y. H., Kim, Y. M., & Kim, B. W. (2003). Cloning and characterization of an exoinulinase from Bacillus polymyxa. Biotechnology Letters, 25(2), 155–159.

    Article  CAS  Google Scholar 

  19. Rey, M. W., Ramaiya, P., Nelson, B. A., Brody-Karpin, S. D., Zaretsky, E. J., Tang, M., de Leon, A. L., Xiang, H., Gusti, V., Clausen, I. G., & Olsen, P. B. (2004). Complete genome sequence of the industrial bacterium Bacillus licheniformis and comparisons with closely related bacillus species. Genome Biology, 5(10), 77.

    Article  Google Scholar 

  20. Schell, M. A., Karmirantzou, M., Snel, B., Vilanova, D., Berger, B., Pessi, G., Zwahlen, M. C., Desiere, F., Bork, P., Delley, M., & Pridmore, R. D. (2002). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proceedings of the National Academy of Sciences, 99(22), 14422–14427.

    Article  CAS  Google Scholar 

  21. Kim, K. Y., Koo, B. S., JO, D., & Kim, S. I. (2004). Cloning, expression, and purification of exoinulinase from Bacillus sp. snu-7. Journal of Microbiology and Biotechnology, 14(2), 344–349.

    CAS  Google Scholar 

  22. 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. Applied Microbiology and Biotechnology, 62(2–3), 180–185.

    Article  CAS  Google Scholar 

  23. Barranco-Florido, E., Garcia-Garibay, M., Gómez-Ruiz, L., & Azaola, A. (2001). Immobilization system of Kluyveromyces marxianus cells in barium alginate for inulin hydrolysis. Process Biochemistry, 37(5), 513–519.

    Article  Google Scholar 

  24. Moriyama, S., Tanaka, H., Uwataki, M., Muguruma, M., & Ohta, K. (2003). Molecular cloning and characterization of an exoinulinase gene from Aspergillus niger strain 12 and its expression in Pichia pastoris. Journal of Bioscience and Bioengineering, 96(4), 324–331.

    Article  CAS  Google Scholar 

  25. Young-man, K., Kim, H. Y., & Choi, Y. J. (2000). Cloning and characterization of Pseudomonas mucidolens exoinulinase. Journal of Microbiology and Biotechnology, 10(2), 238–243.

    Google Scholar 

  26. Liebl, W., Brem, D., & Gotschlich, A. (1998). Analysis of the gene for β-fructosidase (invertase, inulinase) of the hyperthermophilic bacterium Thermotoga maritima, and characterisation of the enzyme expressed in Escherichia coli. Applied Microbiology and Biotechnology, 50(1), 55–64.

    Article  CAS  Google Scholar 

  27. Arand, M., Golubev, A. M., Neto, J. B., Polikarpov, I., Wattiez, R., Korneeva, O. S., Eneyskaya, E. V., Kulminskaya, A. A., Shabalin, K. A., Shishliannikov, S. M., & Chepurnaya, O. V. (2002). Purification, characterization, gene cloning and preliminary X-ray data of the exo-inulinase from Aspergillus awamori. Biochemical Journal, 362(1), 131–135.

    Article  CAS  Google Scholar 

  28. Uhm, T. B., Chae, K. S., Lee, D. W., Kim, H. S., Cassart, J. P., & Vandenhaute, J. (1998). Cloning and nucleotide sequence of the endoinulinase-encoding gene, inu2, from Aspergillus ficuum. Biotechnology Letters, 20(8), 809–812.

    Article  CAS  Google Scholar 

  29. Kang, S. I., Chang, Y. J., Oh, S. J., & Kim, S. I. (1998). Purification and properties of an endo-inulinase from an Arthrobacter sp. Biotechnology Letters, 20(10), 983–986.

    Article  CAS  Google Scholar 

  30. Ohta, K., Akimoto, H., Matsuda, S., Toshimitsu, D., & Nakamura, T. (1998). Molecular cloning and sequence analysis of two endoinulinase genes from Aspergillus niger. Bioscience, Biotechnology, and Biochemistry, 62(9), 1731–1738.

    Article  CAS  Google Scholar 

  31. Akimoto, H., Kiyota, N., Kushima, T., & Nakamura, T. (2000). Molecular cloning and sequence analysis of an endoinulinase gene from Penicillium sp. strain TN-88. Bioscience, Biotechnology, and Biochemistry, 64(11), 2328–2335.

    Article  CAS  Google Scholar 

  32. Onodera, S., Murakami, T., Ito, H., Mori, H., Matsui, H., Honma, M., Chiba, S., & Shiomi, N. (1996). Molecular cloning and nucleotide sequences of cDNA and gene encoding endo-inulinase from Penicillium purpurogenum. Bioscience, Biotechnology, and Biochemistry, 60(11), 1780–1785.

    Article  CAS  Google Scholar 

  33. Slavin, J. (2013). Fiber and prebiotics: mechanisms and health benefits. Nutrients, 5, 1417–1435.

    Article  CAS  Google Scholar 

  34. Biedrzycka, E., & Bielecka, M. (2004). Prebiotic effectiveness of fructans of different degrees of polymerization. Trends in Food Science & Technology, 15(3), 170–175.

    Article  CAS  Google Scholar 

  35. Vera, C., Córdova, A., Aburto, C., Guerrero, C., Suárez, S., & Illanes, A. (2016). Synthesis and purification of galactooligosaccharides: state of the art. World Journal of Microbiology and Biotechnology, 32(12), 197.

    Article  CAS  Google Scholar 

  36. Monteagudo-Mera, A., Arthur, J. C., Jobin, C., Keku, T., Bruno-Barcena, J. M., & Azcarate-Peril, M. A. (2016). High purity galactooligosaccharides enhance specific Bifidobacterium species and their metabolic activity in the mouse gut microbiome. Beneficial Microbes, 7(2), 247–264.

    Article  CAS  Google Scholar 

  37. Bhatia, S., Prabhu, P. N., Benefiel, A. C., Miller, M. J., Chow, J., Davis, S. R., & Gaskins, H. R. (2015). Galacto-oligosaccharides may directly enhance intestinal barrier function through the modulation of goblet cells. Molecular Nutrition & Food Research, 59(3), 566–573.

    Article  CAS  Google Scholar 

  38. Fanaro, S., Boehm, G., Garssen, J., Knol, J., Mosca, F., Stahl, B., & Vigi, V. (2005). Galacto-oligosaccharides and long-chain fructo-oligosaccharides as prebiotics in infant formulas: a review. Acta Paediatrica, 94(s449), 22–26.

    Article  Google Scholar 

  39. Nabarlatz, D., Ebringerová, A., & Montané, D. (2007). Autohydrolysis of agricultural by-products for the production of xylooligosaccharides. Carbohydrate Polymers, 69(1), 20–28.

    Article  CAS  Google Scholar 

  40. Al-Sheraji, S. H., Ismail, A., Manap, M. Y., Mustafa, S., Yusof, R. M., & Hassan, F. A. (2013). Prebiotics as functional foods: a review. Journal of Functional Foods, 5(4), 1542–1553.

    Article  CAS  Google Scholar 

  41. Crittenden, R. G., & Playne, M. (1996). Production, properties and applications of food-grade oligosaccharides. Trends in Food Science & Technology, 7(11), 353–361.

    Article  CAS  Google Scholar 

  42. Niu, D., Qiao, J., Li, P., Tian, K., Liu, X., Singh, S., & Lu, F. (2017). Highly efficient enzymatic preparation of isomaltooligosaccharides from starch using an enzyme cocktail. Electronic Journal of Biotechnology, 26, 46–51.

    Article  CAS  Google Scholar 

  43. Basu, A., Mutturi, S., & Prapulla, S. G. (2016). Production of isomaltooligosaccharides (IMO) using simultaneous saccharification and transglucosylation from starch and sustainable sources. Process Biochemistry, 51(10), 1464–1471.

    Article  CAS  Google Scholar 

  44. Kuriki, T., Yanase, M., Takata, H., Takesada, Y., Imanaka, T., & Okada, S. (1993). A new way of producing isomaltooligosaccharide syrup by using the transglycosylation reaction of neopullulanase. Applied and Environmental Microbiology, 59(4), 953–959.

    CAS  Google Scholar 

  45. Sharma, M., Patel, S. N., Lata, K., Singh, U., Krishania, M., Sangwan, R. S., & Singh, S. P. (2016). A novel approach of integrated bioprocessing of cane molasses for production of prebiotic and functional bioproducts. Bioresource Technology, 219, 311–318.

    Article  CAS  Google Scholar 

  46. Iliev, I., Vassileva, T., Ignatova, C., Ivanova, I., Haertle, T., Monsan, P., & Chobert, J. M. (2008). Gluco-oligosaccharides synthesized by glucosyltransferases from constitutive mutants of Leuconostoc mesenteroides strain Lm 28. Journal of Applied Microbiology, 104(1), 243–250.

    CAS  Google Scholar 

  47. Van Hijum, S. A., Kralj, S., Ozimek, L. K., Dijkhuizen, L., & van Geel-Schutten, I. G. (2006). Structure-function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiology and Molecular Biology Reviews, 70(1), 157–176.

    Article  CAS  Google Scholar 

  48. Robyt, J. F., Yoon, S. H., & Mukerjea, R. (2008). Dextransucrase and the mechanism for dextran biosynthesis. Carbohydrate Research, 343(18), 3039–3048.

    Article  CAS  Google Scholar 

  49. Kubik, C., Sikora, B., & Bielecki, S. (2004). Immobilization of dextransucrase and its use with soluble dextranase for glucooligosaccharides synthesis. Enzyme and Microbial Technology, 34(6), 555–560.

    Article  CAS  Google Scholar 

  50. Goulas, A. K., Cooper, J. M., Grandison, A. S., & Rastall, R. A. (2004). Synthesis of isomaltooligosaccharides and oligodextrans in a recycle membrane bioreactor by the combined use of dextransucrase and dextranase. Biotechnology and Bioengineering, 88(6), 778–787.

    Article  CAS  Google Scholar 

  51. Mussatto, S. I., & Mancilha, I. M. (2007). Non-digestible oligosaccharides: a review. Carbohydrate Polymers, 68(3), 587–597.

    Article  CAS  Google Scholar 

  52. Fujimoto, Y., Hattori, T., Uno, S., Murata, T., & Usui, T. (2009). Enzymatic synthesis of gentiooligosaccharides by transglycosylation with β-glycosidases from Penicillium multicolor. Carbohydrate Research, 344(8), 972–978.

    Article  CAS  Google Scholar 

  53. Kothari, D., & Goyal, A. (2015). Gentiooligosaccharides from Leuconostoc mesenteroides NRRL B-1426 dextransucrase as prebiotics and as a supplement for functional foods with anti-cancer properties. Food & Function, 6(2), 604–611.

    Article  CAS  Google Scholar 

  54. Nanjo, F., Usui, T., & SUZKI, T. (1984). Mode of action of an exo-β-(1→ 3)-D-glucanase on the laminaran from Eisenia bicyclis. Agricultural and biological chemistry., 48(6), 1523–1532.

    CAS  Google Scholar 

  55. Bouhnik, Y., Raskine, L., Simoneau, G., Vicaut, E., Neut, C., Flourié, B., Brouns, F., & Bornet, F. R. (2004). The capacity of nondigestible carbohydrates to stimulate fecal Bifidobacteria in healthy humans: a double-blind, randomized, placebo-controlled, parallel-group, dose-response relation study. The American Journal of Clinical Nutrition, 80(6), 1658–1664.

    CAS  Google Scholar 

  56. Nurhayati, Y., Manaf, A. A., Osman, H., Abdullah, A. B. C., & Tang, J. Y. H. (2016). Effect of chitosan oligosaccharides on the growth of bifidobacterium species. Malaysian Journal of Applied Sciences, 1(1), 13–23.

    Google Scholar 

  57. Zou, P., Yang, X., Wang, J., Li, Y., Yu, H., Zhang, Y., & Liu, G. (2016). Advances in characterisation and biological activities of chitosan and chitosan oligosaccharides. Food Chemistry, 190, 1174–1181.

    Article  CAS  Google Scholar 

  58. Muñoz-Almagro, N., Montilla, A., Moreno, F. J., & Villamiel, M. (2017). Modification of citrus and apple pectin by power ultrasound: effects of acid and enzymatic treatment. Ultrasonics Sonochemistry, 38, 807–819.

    Article  CAS  Google Scholar 

  59. Gómez, B., Gullón, B., Yáñez, R., Schols, H., & Alonso, J. L. (2016). Prebiotic potential of pectins and pectic oligosaccharides derived from lemon peel wastes and sugar beet pulp: a comparative evaluation. Journal of Functional Foods, 20, 108–121.

    Article  CAS  Google Scholar 

  60. Gómez, B., Yáñez, R., Parajó, J. C., & Alonso, J. L. (2016). Production of pectin-derived oligosaccharides from lemon peels by extraction, enzymatic hydrolysis and membrane filtration. Journal of Chemical Technology and Biotechnology, 91(1), 234–247.

    Article  CAS  Google Scholar 

  61. Holck, J., Lorentzen, A., Vigsnæs, L. K., Licht, T. R., Mikkelsen, J. D., & Meyer, A. S. (2011). Feruloylated and nonferuloylated arabinooligosaccharides from sugar beet pectin selectively stimulate the growth of Bifidobacterium spp. in human fecal in vitro fermentations. Journal of Agricultural and Food Chemistry, 59(12), 6511–6519.

    Article  CAS  Google Scholar 

  62. Margolles, A., & Clara, G. (2003). Purification and functional characterization of a novel α-l-arabinofuranosidase from Bifidobacterium longum B667. Applied and Environmental Microbiology, 69(9), 5096–5103.

    Article  CAS  Google Scholar 

  63. Sulek, K., Vigsnaes, L. K., Schmidt, L. R., Holck, J., Frandsen, H. L., Smedsgaard, J., Skov, T. H., Meyer, A. S., & Licht, T. R. (2014). A combined metabolomic and phylogenetic study reveals putatively prebiotic effects of high molecular weight arabinooligosaccharides when assessed by in vitro fermentation in bacterial communities derived from humans. Anaerobe, 28, 68–77.

    Article  CAS  Google Scholar 

  64. Rastall, R. A., & Maitin, V. (2002). Prebiotics and synbiotics: towards the next generation. Current Opinion in Biotechnology, 13(5), 490–496.

    Article  CAS  Google Scholar 

  65. Hu, B., Gong, Q., Wang, Y., Ma, Y., Li, J., & Yu, W. (2006). Prebiotic effects of neoagarooligosaccharides prepared by enzymatic hydrolysis of agarose. Anaerobe, 12(5), 260–266.

    Article  CAS  Google Scholar 

  66. Li, M., Li, G., Zhu, L., Yin, Y., Zhao, X., Xiang, C., Yu, G., & Wang, X. (2014). Isolation and characterization of an agarooligosaccharide (AO)-hydrolyzing bacterium from the gut microflora of Chinese individuals. PloS One, 9(3), e91106.

    Article  CAS  Google Scholar 

  67. Qiu, D., Vuong, T., Valliyodan, B., Shi, H., Guo, B., Shannon, J. G., & Nguyen, H. T. (2015). Identification and characterization of a stachyose synthase gene controlling reduced stachyose content in soybean. Theoretical and Applied Genetics, 128(11), 2167–2176.

    Article  CAS  Google Scholar 

  68. Song, Y. S., Lee, H. U., Park, C., & Kim, S. W. (2013). Optimization of lactulose synthesis from whey lactose by immobilized β-galactosidase and glucose isomerase. Carbohydrate Research, 369, 1–5.

    Article  CAS  Google Scholar 

  69. Silveira, M. F., Masson, L. M. P., Martins, J. F. P., Álvares, T. D. S., Paschoalin, V. M. F., Lázaro de la Torre, C. & Conte-Junior, C. A. (2015). Simultaneous determination of lactulose and lactose in conserved milk by HPLC-RID. Journal of Chemistry, 2015(2015), 1–6.

  70. Duarte, L. S., da Natividade Schöffer, J., Lorenzoni, A. S. G., Rodrigues, R. C., Rodrigues, E. & Hertz, P. F. (2017). A new bioprocess for the production of prebiotic lactosucrose by an immobilized β-galactosidase. Process Biochemistry, 55, 96–103.

  71. Mu, W., Chen, Q., Wang, X., Zhang, T., & Jiang, B. (2013). Current studies on physiological functions and biological production of lactosucrose. Applied Microbiology and Biotechnology, 97(16), 7073–7080.

    Article  CAS  Google Scholar 

  72. Bali, V., Panesar, P. S., Bera, M. B., & Panesar, R. (2015). Fructooligosaccharides: production, purification and potential applications. Critical Reviews in Food Science and Nutrition, 55(11), 1475–1490.

    Article  CAS  Google Scholar 

  73. Casci, T., & Rastall, R. A. (2006). Manufacture of prebiotic oligosaccharides (pp. 29–55). Prebiotics: Development and applications, New York, John Wiley.

    Google Scholar 

  74. Campbell, J. M., Bauer, L. L., Fahey, G. C., Hogarth, A. J. C. L., Wolf, B. W., & Hunter, D. E. (1997). Selected fructooligosaccharide (1-kestose, nystose, and 1F-β-fructofuranosylnystose) composition of foods and feeds. Journal of Agricultural and Food Chemistry, 45(8), 3076–3082.

    Article  CAS  Google Scholar 

  75. Montet, D., & Ray, R. C. (2016). Fermented foods. Biochemistry and biotechnology. New York, NY: CRC Press.

    Google Scholar 

  76. Wang, J., Sporns, P., & Low, N. H. (1999). Analysis of food oligosaccharides using MALDI-MS: quantification of fructooligosaccharides. Journal of Agricultural and Food Chemistry, 47(4), 1549–1557.

    Article  CAS  Google Scholar 

  77. Roberfroid, M., & Slavin, J. (2000). Nondigestible oligosaccharides. Critical Reviews in Food Science and Nutrition, 40(6), 461–480.

    Article  CAS  Google Scholar 

  78. Bornet, F. R. J. (1994). Undigestible sugars in food products. The American Journal of Clinical Nutrition, 59(3), 763–769.

    Google Scholar 

  79. Linde, D., Rodríguez-Colinas, B., Estévez, M., Poveda, A., Plou, F. J., & Lobato, M. F. (2012). Analysis of neofructooligosaccharides production mediated by the extracellular β-fructofuranosidase from Xanthophyllomyces dendrorhous. Bioresource Technology, 109, 123–130.

    Article  CAS  Google Scholar 

  80. Kilian, S., Kritzinger, S., Rycroft, C., Gibson, G., & Du Preez, J. (2002). The effects of the novel bifidogenic trisaccharide, neokestose, on the human colonic microbiota. World Journal of Microbiology and Biotechnology, 18(7), 637–644.

    Article  CAS  Google Scholar 

  81. Trujillo, L. E., Arrieta, J. G., Dafhnis, F., Garcıa, J., Valdes, J., Tambara, Y., & Hernández, L. (2001). Fructooligosaccharides production by the Gluconacetobacter diazotrophicus levansucrase expressed in the methylotrophic yeast Pichia pastoris. Enzyme and Microbial Technology, 28(2), 139–144.

    Article  CAS  Google Scholar 

  82. Bhatia, I. S., & Nandra, K. S. (1979). Studies on fructosyl transferase from Agave americana. Phytochemistry, 18(6), 923–927.

    Article  CAS  Google Scholar 

  83. Mellado-Mojica, E., de la Vara, L. E. G., & López, M. G. (2016). Fructan active enzymes (FAZY) activities and biosynthesis of fructooligosaccharides in the vacuoles of Agave tequilana Weber Blue variety plants of different age. Planta, 245(2), 265–281.

    Article  CAS  Google Scholar 

  84. Bhatia, I. S., Satyanarayana, M. N., & Srinivasan, M. (1955). Transfructosidase from Agave vera cruz Mill. Biochemical Journal, 61(1), 171.

    Article  CAS  Google Scholar 

  85. Henry, R. J., & Darbyshire, B. (1980). Sucrose: Sucrose fructosyltransferase and fructan: Fructan fructosyltransferase from Allium cepa. Phytochemistry, 19(6), 1017–1020.

    Article  CAS  Google Scholar 

  86. Verhaest, M., Le Roy, K., Sansen, S., De Coninck, B., Lammens, W., De Ranter, C. J., Van Laere, A., Van den Ende, W., & Rabijns, A. (2005). Crystallization and preliminary X-ray diffraction study of a cell-wall invertase from Arabidopsis thaliana. Acta Crystallographica Section F: Structural Biology and Crystallization Communications, 61(8), 766–768.

    CAS  Google Scholar 

  87. Shiomi, N. (1982). Purification and characterisation of 1F-fructosyltransferase from the roots of asparagus (Asparagus officinalis L.) Carbohydrate Research, 99(2), 157–169.

    Article  CAS  Google Scholar 

  88. Lüscher, M., Hochstrasser, U., Boller, T., & Wiemken, A. (2000). Isolation of sucrose: sucrose 1-fructosyltransferase (1-SST) from barley (Hordeum vulgare). New Phytologist, 145(2), 225–232.

    Article  Google Scholar 

  89. Singh, R., & Bhatia, I. S. (1971). Isolation and characterization of fructosyltransferase from chicory roots. Phytochemistry, 10(3), 495–502.

    Article  CAS  Google Scholar 

  90. Edelman, J., & Jeeeord, T. G. (1968). The mechanisim of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus. New Phytologist, 67(3), 517–531.

    Article  CAS  Google Scholar 

  91. Chandorkar, K. R., & Collins, F. W. (1972). De novo synthesis of fructooligosaccharides in leaf disks of certain Asteraceae. Canadian Journal of Botany, 50(2), 295–303.

    Article  CAS  Google Scholar 

  92. Abeynayake, S. W., Byrne, S., Nagy, I., Jonavičienė, K., Etzerodt, T. P., Boelt, B., & Asp, T. (2015). Changes in Lolium perenne transcriptome during cold acclimation in two genotypes adapted to different climatic conditions. BMC Plant Biology, 15(1), 250.

    Article  CAS  Google Scholar 

  93. Nagamatsu, Y., Yahata, M., Fukada, T., & Hatanaka, C. (1990). Identification of 1-kestose and neokestose based oligofruetans in Lycoris radiata herb tissues. Agricultural and Biological Chemistry, 54(5), 1291–1292.

    CAS  Google Scholar 

  94. Tamura, K. I., Sanada, Y., Tase, K., & Yoshida, M. (2014). Fructan metabolism and expression of genes coding fructan metabolic enzymes during cold acclimation and overwintering in timothy (Phleum pratense). Journal of Plant Physiology, 171(11), 951–958.

    Article  CAS  Google Scholar 

  95. Barreteau, H., Delattre, C., & Michaud, P. (2006). Production of oligosaccharides as promising new food additive generation. Food Technology and Biotechnology, 44(3), 323.

    CAS  Google Scholar 

  96. Jiang, H., Ma, Y., Chi, Z., Liu, G. L., & Chi, Z. M. (2016). Production, purification, and gene cloning of a β-fructofuranosidase with a high inulin-hydrolyzing activity produced by a novel yeast Aureobasidium sp. P6 isolated from a mangrove ecosystem. Marine Biotechnology, 18(4), 500–510.

    Article  CAS  Google Scholar 

  97. Ghazi, I., Fernandez-Arrojo, L., Garcia-Arellano, H., Ferrer, M., Ballesteros, A., & Plou, F. J. (2007). Purification and kinetic characterization of a fructosyltransferase from Aspergillus aculeatus. Journal of Biotechnology, 128(1), 204–211.

    Article  CAS  Google Scholar 

  98. Ganaie, M. A., Gupta, U. S., & Kango, N. (2013). Screening of biocatalysts for transformation of sucrose to fructooligosaccharides. Journal of Molecular Catalysis B: Enzymatic, 97, 12–17.

    Article  CAS  Google Scholar 

  99. Hang, Y. D., Woodams, E. E., & Jang, K. Y. (1995). Enzymatic conversion of sucrose to kestose by fungal extracellular fructosyltransferase. Biotechnology Letters, 17(3), 295–298.

    Article  CAS  Google Scholar 

  100. Chen, W. C., & Liu, C. H. (1996). Production of β-fructofuranosidase by Aspergillus japonicus. Enzyme and Microbial Technology, 18(2), 153–160.

    Article  CAS  Google Scholar 

  101. L’Hocine, L., Wang, Z., Jiang, B., & Xu, S. (2000). Purification and partial characterization of fructosyltransferase and invertase from Aspergillus niger AS0023. Journal of Biotechnology, 81(1), 73–84.

    Article  Google Scholar 

  102. Murakami, H., Muroi, H., Kuramoto, T., Tamura, Y., Mizutani, K., Nakano, H., & Kitahata, S. (1990). Purification and some properties of a levanase from Streptomyces sp. no. 7–3. Agricultural and Biological Chemistry, 54(9), 2247–2255.

    CAS  Google Scholar 

  103. Van Balken, J. A. M., Van Dooren, T. J., Van den Tweel, W. J. J., Kamphuis, J., & Meijer, E. M. (1991). Production of 1-kestose with intact mycelium of Aspergillus phoenicis containing sucrose-1F-fructosyltransferase. Applied Microbiology and Biotechnology, 35(2), 216–221.

    Article  Google Scholar 

  104. Muramatsu, M., & Nakakuki, T. (1995). Enzymatic synthesis of novel fructosyl and oligofructosyl trehaloses by Aspergillus sydowi β-fructofuranosidase. Bioscience, Biotechnology, and Biochemistry, 59(2), 208–212.

    Article  CAS  Google Scholar 

  105. Yun, J. W., Kim, D. H., & Song, S. K. (1997). Enhanced production of fructosyltransferase and glucosyltransferase by substrate-feeding cultures of Aureobasidium pullulans. Journal of Fermentation and Bioengineering, 84(3), 261–263.

    Article  CAS  Google Scholar 

  106. Lim, J. S., Park, M. C., Lee, J. H., Park, S. W., & Kim, S. W. (2005). Optimization of culture medium and conditions for neo-fructooligosaccharides production by Penicillium citrinum. European Food Research and Technology, 221(5), 639–644.

    Article  CAS  Google Scholar 

  107. Dhake, A. B., & Patil, M. B. (2007). Effect of substrate feeding on production of fructosyltransferase by Penicillium purpurogenum. Brazilian Journal of Microbiology, 38(2), 194–199.

    Article  Google Scholar 

  108. Barthomeuf, C., & Pourrat, H. (1995). Production of high-content fructooligosaccharides by an enzymatic system from Penicillium rugulosum. Biotechnology Letters, 17(9), 911–916.

    Article  CAS  Google Scholar 

  109. Hernalsteens, S., & Maugeri, F. (2010). Synthesis of fructooligosaccharides using extracellular enzymes from Rhodotorula sp. Journal of Food Biochemistry, 34(3), 520–534.

    CAS  Google Scholar 

  110. Linde, D., Macias, I., Fernández-Arrojo, L., Plou, F. J., Jiménez, A., & Fernández-Lobato, M. (2009). Molecular and biochemical characterization of a β-fructofuranosidase from Xanthophyllomyces dendrorhous. Applied and Environmental Microbiology, 75(4), 1065–1073.

    Article  CAS  Google Scholar 

  111. Bergeron, L. J., Morou-Bermudez, E., & Burne, R. A. (2000). Characterization of the fructosyltransferase gene of Actinomyces naeslundii WVU45. Journal of Bacteriology, 182(13), 3649–3654.

    Article  CAS  Google Scholar 

  112. Pabst, M. J. (1977). Levan and levansucrase of Actinomyces viscosus. Infection and Immunity, 15(2), 518–526.

    CAS  Google Scholar 

  113. Tonozuka, T., Tamaki, A., Yokoi, G., Miyazaki, T., Ichikawa, M., Nishikawa, A., & Ito, T. (2012). Crystal structure of a lactosucrose-producing enzyme, Arthrobacter sp. K-1 β-fructofuranosidase. Enzyme and Microbial Technology, 51(6), 359–365.

    Article  CAS  Google Scholar 

  114. Olivares-Illana, V., López-Munguía, A., & Olvera, C. (2003). Molecular characterization of inulosucrase from Leuconostoc citreum: a fructosyltransferase within a glucosyltransferase. Journal of Bacteriology, 185(12), 3606–3612.

    Article  CAS  Google Scholar 

  115. Woo Kim, B., Won Choi, J., & Won Yun, J. (1998). Selective production of GF4-fructooligosaccharide from sucrose by a new transfructosylating enzyme. Biotechnology Letters, 20(11), 1031–1034.

    Article  Google Scholar 

  116. Korneli, C., Biedendieck, R., David, F., Jahn, D., & Wittmann, C. (2013). High yield production of extracellular recombinant levansucrase by Bacillus megaterium. Applied Microbiology and Biotechnology, 97(8), 3343–3353.

    Article  CAS  Google Scholar 

  117. Zhang, T., Li, R., Qian, H., Mu, W., Miao, M., & Jiang, B. (2014). Biosynthesis of levan by levansucrase from Bacillus methylotrophicus SK 21.002. Carbohydrate Polymers, 101, 975–981.

    Article  CAS  Google Scholar 

  118. Gay, P., Chalumeau, H., & Steinmetz, M. (1983). Chromosomal localization of gut, fruC, and pfk mutations affecting genes involved in Bacillus subtilis D-glucitol catabolism. Journal of Bacteriology, 153(3), 1133–1137.

    CAS  Google Scholar 

  119. Vaidya, V. D., & Prasad, D. T. (2012). Thermostable levansucrase from Bacillus subtilis BB04, an isolate of banana peel. Journal of Biochemical Technology, 3(4), 322–327.

    CAS  Google Scholar 

  120. Abdel-Fattah, A. F., Mahmoud, D. A., & Esawy, M. A. (2005). Production of levansucrase from Bacillus subtilis NRC 33a and enzymic synthesis of levan and fructooligosaccharides. Current Microbiology, 51(6), 402–407.

    Article  CAS  Google Scholar 

  121. Liu, Q., Yu, S., Zhang, T., Jiang, B., & Mu, W. (2017). Efficient biosynthesis of levan from sucrose by a novel levansucrase from Brenneria goodwinii. Carbohydrate Polymers, 157, 1732–1740.

    Article  CAS  Google Scholar 

  122. Looten, P., Blanchet, D., & Vandecasteele, J. P. (1987). The β-fructofuranosidase activities of a strain of Clostridium acetobutylicum grown on inulin. Applied Microbiology and Biotechnology, 25(5), 419–425.

    Article  CAS  Google Scholar 

  123. Seibel, J., Moraru, R., Götze, S., Buchholz, K., Na’amnieh, S., Pawlowski, A., & Hecht, H. J. (2006). Synthesis of sucrose analogues and the mechanism of action of Bacillus subtilis fructosyltransferase (levansucrase). Carbohydrate Research, 341(14), 2335–2349.

    Article  CAS  Google Scholar 

  124. Gross, M., Geier, G., Rudolph, K., & Geider, K. (1992). Levan and levansucrase synthesized by the fireblight pathogen Erwinia amylovora. Physiological and Molecular Plant Pathology, 40(6), 371–381.

    Article  CAS  Google Scholar 

  125. Chambert, R., & Petit-Glatron, M. F. (1991). Polymerase and hydrolase activities of Bacillus subtilis levansucrase can be separately modulated by site-directed mutagenesis. Biochemical Journal, 279(1), 35–41.

    Article  CAS  Google Scholar 

  126. Tieking, M., Korakli, M., Ehrmann, M. A., Gänzle, M. G., & Vogel, R. F. (2003). In situ production of exopolysaccharides during sourdough fermentation by cereal and intestinal isolates of lactic acid bacteria. Applied and Environmental Microbiology, 69(2), 945–952.

    Article  CAS  Google Scholar 

  127. Waldherr, F. W., Meissner, D., & Vogel, R. F. (2008). Genetic and functional characterization of Lactobacillus panis levansucrase. Archives of Microbiology, 190(4), 497.

    Article  CAS  Google Scholar 

  128. Van Hijum, S. A. F. T., Szalowska, E., Van Der Maarel, M. J. E. C., & Dijkhuizen, L. (2004). Biochemical and molecular characterization of a levansucrase from Lactobacillus reuteri. Microbiology, 150(3), 621–630.

    Article  CAS  Google Scholar 

  129. Han, J., Xu, X., Gao, C., Liu, Z., & Wu, Z. (2016). Levan-producing Leuconostoc citreum strain BD1707 and its growth in tomato juice supplemented with sucrose. Applied and Environmental Microbiology, 82(5), 1383–1390.

    Article  CAS  Google Scholar 

  130. Beine, R., Moraru, R., Nimtz, M., Na’amnieh, S., Pawlowski, A., Buchholz, K., & Seibel, J. (2008). Synthesis of novel fructooligosaccharides by substrate and enzyme engineering. Journal of Biotechnology, 138(1), 33–41.

    Article  CAS  Google Scholar 

  131. Xu, X., Gao, C., Liu, Z., Wu, J., Han, J., Yan, M., & Wu, Z. (2016). Characterization of the levan produced by Paenibacillus bovis sp. nov BD3526 and its immunological activity. Carbohydrate Polymers, 144, 178–186.

    Article  CAS  Google Scholar 

  132. Youssef, G. A., Youssef, A. S., Talha, S., & El-Aassar, S. A. (2014). Increased fructosyltranseferase (levansucrase) production by optimizing culture condition from Pediococcus acidilactici strain in shaking batch cultures. Life Science Journal, 11(7), 33–47.

    Google Scholar 

  133. Hettwer, U., Gross, M., & Rudolph, K. (1995). Purification and characterization of an extracellular levansucrase from Pseudomonas syringae pv. Phaseolicola. Journal of Bacteriology, 177(10), 2834–2839.

    Article  CAS  Google Scholar 

  134. Ohtsuka, K., Hino, S., Fukushima, T., Ozawa, O., Kanematsu, T., & Uchida, T. (1992). Characterization of levansucrase from Rahnella aquatilis JCM-1683. Bioscience, Biotechnology, and Biochemistry, 56(9), 1373–1377.

    Article  CAS  Google Scholar 

  135. Schroeder, V. A., Michalek, S. M., & Macrina, F. L. (1989). Biochemical characterization and evaluation of virulence of a fructosyltransferase-deficient mutant of Streptococcus mutans V403. Infection and Immunity, 57(11), 3560–3569.

    CAS  Google Scholar 

  136. Song, D. D., & Jacques, N. A. (1999). Mutation of aspartic acid residues in the fructosyltrans- ferase of Streptococcus salivarius ATCC 25975. Biochemical Journal, 344(1), 259–264.

    CAS  Google Scholar 

  137. Bekers, M., Laukevics, J., Upite, D., Kaminska, E., Vigants, A., Viesturs, U., Pankova, L., & Danilevics, A. (2002). Fructooligosaccharide and levan producing activity of Zymomonas mobilis extracellular levansucrase. Process Biochemistry, 38(5), 701–706.

    Article  CAS  Google Scholar 

  138. Antosova, M., & Polakovic, M. (2002). Fructosyltransferases: the enzymes catalyzing production of fructooligosaccharides. Chemical papers-slovak Academy of Sciences, 55(6), 350–358.

    Google Scholar 

  139. Fernandez, R. C., Ottoni, C. A., Da Silva, E. S., Matsubara, R. M. S., Carter, J. M., Magossi, L. R., Wada, M. A. A., de Andrade Rodrigues, M. F., Maresma, B. G., & Maiorano, A. E. (2007). Screening of β-fructofuranosidase-producing microorganisms and effect of pH and temperature on enzymatic rate. Applied Microbiology and Biotechnology, 75(1), 87–93.

    Article  CAS  Google Scholar 

  140. Hendry, G. A. (1993). Evolutionary origins and natural functions of fructans - a climatological, biogeographic and mechanistic appraisal. New Phytologist, 123(1), 3–14.

    Article  CAS  Google Scholar 

  141. Livingston, D. P., Hincha, D. K., & Heyer, A. G. (2009). Fructan and its relationship to abiotic stress tolerance in plants. Cellular and Molecular Life Sciences, 66(13), 2007–2023.

    Article  CAS  Google Scholar 

  142. van Arkel, J., Sévenier, R., Hakkert, J. C., Bouwmeester, H. J., Koops, A. J., & van der Meer, I. M. (2013). Tailor-made fructan synthesis in plants: a review. Carbohydrate. Polymer., 93, 48–56.

    Article  CAS  Google Scholar 

  143. Koops, A. J., & Jonker, H. H. (1994). Purification and characterization of the enzymes of fructan biosynthesis in tubers of Helianthus tuberosus ‘Colombia’I. Fructan: fructan fructosyl transferase. Journal of Experimental Botany, 45(11), 1623–1631.

    Article  CAS  Google Scholar 

  144. Ende, W. V., Michiels, A., Roover, J. D., & Laere, A. (2002). Fructan biosynthetic and breakdown enzymes in dicots evolved from different invertases. Expression of fructan genes throughout chicory development. The Scientific World Journal, 2, 1281–1295.

    Article  CAS  Google Scholar 

  145. Altenbach, D., Nüesch, E., Meyer, A. D., Boller, T., & Wiemken, A. (2004). The large subunit determines catalytic specificity of barley sucrose: fructan 6-fructosyltransferase and fescue sucrose: sucrose 1-fructosyltransferase. FEBS Letters, 567(2–3), 214–218.

    Article  CAS  Google Scholar 

  146. Eggleston, G., & Cote, G. L. (2003). Oligosaccharides in food and agriculture. ACS Symposium Series, 849. Chapter, 1, 1–14. https://doi.org/10.1021/bk-2003-0849.ch001.

    Google Scholar 

  147. Fujishima, M., Sakai, H., Ueno, K., Takahashi, N., Onodera, S., Benkeblia, N., & Shiomi, N. (2005). Purification and characterization of a fructosyltransferase from onion bulbs and its key role in the synthesis of fructo-oligosaccharides in vivo. New Phytologist, 165(2), 513–524.

    Article  CAS  Google Scholar 

  148. Yesilirmak, F. & Sayers, Z. (2009). Heterelogous expression of plant genes. International Journal of Plant Genomics, 2009, doi.org/10.1155/2009/296482.

  149. Frommer, W. B., & Ninnemann, O. (1995). Heterologous expression of genes in bacterial, fungal, animal, and plant cells. Annual Review of Plant Biology, 46(1), 419–444.

    Article  CAS  Google Scholar 

  150. Dake, M. S., & Kumar, G. (2012). Partial purification and characterization of fructosyltransferase from Aureobasidium pullulans. International Journal of Science, Environment and Technology, 1(2), 88–98.

    Google Scholar 

  151. Seo, E. S., Lee, J. H., Cho, J. Y., Seo, M. Y., Lee, H. S., Chang, S. S., Lee, H. J., Choi, J. S., & Kim, D. (2004). Synthesis and characterization of fructooligosaccharides using levansucrase with a high concentration of sucrose. Biotechnology and Bioprocess Engineering, 9(5), 339–344.

    Article  CAS  Google Scholar 

  152. Olvera, C., Centeno-Leija, S., & López-Munguía, A. (2007). Structural and functional features of fructansucrases present in Leuconostoc mesenteroides ATCC 8293. Antonie Van Leeuwenhoek, 92(1), 11–20.

    Article  CAS  Google Scholar 

  153. Díez-Municio, M., de las Rivas, B., Jimeno, M. L., Muñoz, R., Moreno, F. J., & Herrero, M. (2013). Enzymatic synthesis and characterization of fructooligosaccharides and novel maltosylfructosides by inulosucrase from Lactobacillus gasseri DSM 20604. Applied and Environmental Microbiology, 79(13), 4129–4140.

    Article  CAS  Google Scholar 

  154. Maugeri, F., & Hernalsteens, S. (2007). Screening of yeast strains for transfructosylating activity. Journal of Molecular Catalysis B: Enzymatic, 49(1), 43–49.

    Article  CAS  Google Scholar 

  155. Steinmetz, M., Le Coq, D., Aymerich, S., Gonzy-Tréboul, G., & Gay, P. (1985). The DNA sequence of the gene for the secreted Bacillus subtilis enzyme levansucrase and its genetic control sites. Molecular and General Genetics, 200(2), 220–228.

    Article  CAS  Google Scholar 

  156. Geier, G., & Geider, K. (1993). Characterization and influence on virulence of the levansucrase gene from the fireblight pathogen Erwinia amylovora. Physiological and Molecular Plant Pathology, 42(6), 387–404.

    Article  CAS  Google Scholar 

  157. Arrieta, J., Hernandez, L., Coego, A., Suárez, V., Balmori, E., Menéndez, C., Petit-Glatron, M. F., Chambert, R., & Selman-Housein, G. (1996). Molecular characterization of the levansucrase gene from the endophytic sugarcane bacterium Acetobacter diazotrophicus SRT4. Microbiology, 142(5), 1077–1085.

    Article  CAS  Google Scholar 

  158. Tian, F., Inthanavong, L., & Karboune, S. (2011). Purification and characterization of levansucrases from Bacillus amyloliquefaciens in intra-and extracellular forms useful for the synthesis of levan and fructooligosaccharides. Bioscience, Biotechnology, and Biochemistry, 75(10), 1929–1938.

    Article  CAS  Google Scholar 

  159. Anwar, M. A., Kralj, S., van der Maarel, M. J., & Dijkhuizen, L. (2008). The probiotic Lactobacillus johnsonii NCC 533 produces high-molecular-mass inulin from sucrose by using an inulosucrase enzyme. Applied and Environmental Microbiology, 74(11), 3426–3433.

    Article  CAS  Google Scholar 

  160. Jong, W. Y., & Seung, K. S. (1993). The production of high-content fructooligosaccharides from sucrose by the mixed-enzyme system of fructosyltransferase and glucose oxidase. Biotechnology Letters, 15(6), 573–576.

    Article  Google Scholar 

  161. Dominguez, A. L., Rodrigues, L. R., Lima, N. M., & Teixeira, J. A. (2014). An overview of the recent developments on fructooligosaccharide production and applications. Food and Bioprocess Technology, 7(2), 324–337.

    Article  CAS  Google Scholar 

  162. Wanker, E., Huber, A., & Schwab, H. (1995). Purification and characterization of the Bacillus subtilis levanase produced in Escherichia coli. Applied and Environmental Microbiology, 61(5), 1953–1958.

    CAS  Google Scholar 

  163. Chaudhary, A., Gupta, L. K., Gupta, J. K., & Banerjee, U. C. (1996). Purification and properties of levanase from Rhodotorula sp. Journal of Biotechnology, 46(1), 55–61.

    Article  CAS  Google Scholar 

  164. Takahashi, N., Mizuno, F., & Takamori, K. (1983). Isolation and properties of levanase from Streptococcus salivarius KTA-19. Infection and Immunity, 42(1), 231–236.

    CAS  Google Scholar 

  165. Menéndez, C., Hernández, L., Selman, G., Mendoza, M. F., Hevia, P., Sotolongo, M., & Arrieta, J. G. (2002). Molecular cloning and expression in Escherichia coli of an exo-levanase gene from the endophytic bacterium Gluconacetobacter diazotrophicus SRT4. Current Microbiology, 45(1), 5–12.

    Article  CAS  Google Scholar 

  166. Jensen, S. L., Diemer, M. B., Lundmark, M., Larsen, F. H., Blennow, A., Mogensen, H. K., & Nielsen, T. H. (2016). Levanase from Bacillus subtilis hydrolyses β-2, 6 fructosyl bonds in bacterial levans and in grass fructans. International Journal of Biological Macromolecules, 85, 514–521.

    Article  CAS  Google Scholar 

  167. Silva, M. F., Rigo, D., Mossi, V., Golunski, S., de Oliveira Kuhn, G., Di Luccio, M., Dallago, R., de Oliveira, D., Oliveira, J. V., & Treichel, H. (2013). Enzymatic synthesis of fructooligosaccharides by inulinases from Aspergillus niger and Kluyveromyces marxianus NRRL Y-7571 in aqueous–organic medium. Food Chemistry, 138(1), 148–153.

    Article  CAS  Google Scholar 

  168. Oseguera, M. P., Guereca, L., & Lopez-Munguia, A. (1996). Properties of levansucrase from Bacillus circulans. Applied Microbiology and Biotechnology, 45(4), 465–471.

    Article  CAS  Google Scholar 

  169. Tieking, M., Kaditzky, S., Valcheva, R., Korakli, M., Vogel, R. F., & Gänzle, M. G. (2005). Extracellular homopolysaccharides and oligosaccharides from intestinal lactobacilli. Journal of Applied Microbiology, 99(3), 692–702.

    Article  CAS  Google Scholar 

  170. Baciu, I. E., Jördening, H. J., Seibel, J., & Buchholz, K. (2005). Investigations of the transfructosylation reaction by fructosyltransferase from B. subtilis NCIMB 11871 for the synthesis of the sucrose analogue galactosyl-fructoside. Journal of Biotechnology, 116(4), 347–357.

    Article  CAS  Google Scholar 

  171. Li, W., Yu, S., Zhang, T., Jiang, B., & Mu, W. (2017). Synthesis of raffinose by transfructosylation using recombinant levansucrase from Clostridium arbusti SL206. Journal of the Science of Food and Agriculture, 97(1), 43–49.

    Article  CAS  Google Scholar 

  172. Morales-Arrieta, S., Rodríguez, M. E., Segovia, L., López-Munguía, A., & Olvera-Carranza, C. (2006). Identification and functional characterization of levS, a gene encoding for a levansucrase from Leuconostoc mesenteroides NRRL B-512 F. Gene, 376(1), 59–67.

    Article  CAS  Google Scholar 

  173. Sandkvist, M. (2001). Biology of type II secretion. Molecular Microbiology, 40(2), 271–283.

    Article  CAS  Google Scholar 

  174. Kralj, S. (2004). Glucansucrases of lactobacilli. Journal of Biological Chemistry, 276, 44557–44562.

    Google Scholar 

  175. Nurizzo, D., Turkenburg, J. P., Charnock, S. J., Roberts, S. M., Dodson, E. J., McKie, V. A., Taylor, E. J., Gilbert, H. J., & Davies, G. J. (2002). Cellvibrio japonicus α-L-arabinanase 43A has a novel five-blade β-propeller fold. Nature Structural & Molecular Biology, 9(9), 665–668.

    Article  CAS  Google Scholar 

  176. Meng, G., & Fütterer, K. (2003). Structural framework of fructosyl transfer in Bacillus subtilis levansucrase. Nature Structural & Molecular Biology, 10(11), 935–941.

    Article  CAS  Google Scholar 

  177. Martínez-Fleites, C., Ortíz-Lombardía, M., Pons, T., Tarbouriech, N., Taylor, E. J., Arrieta, J. G., Hernández, L., & Davies, G. J. (2005). Crystal structure of levansucrase from the gram-negative bacterium Gluconacetobacter diazotrophicus. Biochemical Journal, 390(1), 19–27.

    Article  CAS  Google Scholar 

  178. Yanase, H., Maeda, M., Hagiwara, E., Yagi, H., Taniguchi, K., & Okamoto, K. (2002). Identification of functionally important amino acid residues in Zymomonas mobilis levansucrase. Journal of Biochemistry, 132(4), 565–572.

    Article  CAS  Google Scholar 

  179. Flores-Maltos, D. A., Mussatto, S. I., Contreras-Esquivel, J. C., Rodríguez-Herrera, R., Teixeira, J. A., & Aguilar, C. N. (2016). Biotechnological production and application of fructooligosaccharides. Critical Reviews in Biotechnology, 36(2), 259–267.

    Article  CAS  Google Scholar 

  180. Guo, M., Chen, G., & Chen, K. (2016). Fructooligosaccharides: effects, mechanisms, and applications (pp. 51–63). Springer New York: In research progress in oligosaccharins.

    Google Scholar 

  181. Patel, S., & Goyal, A. (2012). The current trends and future perspectives of prebiotics research: a review. 3. Biotech, 2(2), 115–125.

    CAS  Google Scholar 

  182. Dominguez, L. J., Martínez-González, M. A., Basterra-Gortari, F. J., Gea, A., Barbagallo, M., & Bes-Rastrollo, M. (2014). Fast food consumption and gestational diabetes incidence in the SUN project. PloS One, 9(9), e106627.

    Article  CAS  Google Scholar 

  183. Chen, G., Li, C., & Chen, K. (2016). Fructooligosaccharides: A review on their mechanisms of action and effects. Studies in natural products chemistry: Bioactive Natural Products, 48, 209–229.

    Article  Google Scholar 

  184. Gibson, G. R., Beatty, E. R., Wang, X., & Cummings, J. H. (1995). Selective stimulation of bifidobacteria in the human colon by oligofructose and inulin. Gastroenterology, 108(4), 975–982.

    Article  CAS  Google Scholar 

  185. Celligoi, M. A. P. C., dos Santos, D. A., da Silva, P. B., & Baldo, C. (2015). Fermented foods, part I biochemistry and biotechnology. Taylor & Francis Group: CRC Press.

    Google Scholar 

  186. Xiao, J., Sakaguchi, E., & Bai, G. (2016). Short-term supplementation with dietary fructooligosaccharide and dietary mannitol elevated the absorption of calcium and magnesium in adult rats. Czech Journal of Animal Science, 61(6), 281–289.

    Article  Google Scholar 

  187. Coxam, V. (2007). Current data with inulin-type fructans and calcium, targeting bone health in adults. The Journal of Nutrition, 137, 2527S–2533S.

    CAS  Google Scholar 

Download references

Acknowledgements

The authors acknowledge the Department of Biotechnology (DBT), Government of India. JSJ and LKN acknowledges Science and Engineering Research Board (SERB) N-PDF fellowships, PDF/2016/445 and PDF/2015/662, respectively.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Sudhir P. Singh or Ashok Pandey.

Ethics declarations

Conflict of Interest

The authors declare that they have 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

Singh, S.P., Jadaun, J.S., Narnoliya, L.K. et al. Prebiotic Oligosaccharides: Special Focus on Fructooligosaccharides, Its Biosynthesis and Bioactivity. Appl Biochem Biotechnol 183, 613–635 (2017). https://doi.org/10.1007/s12010-017-2605-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12010-017-2605-2

Keywords

Navigation