Microbial FTases produced by filamentous fungi, its activity, and fermentation temperature of the maximum enzyme activity reached.
Abstract
Fructooligosaccharides (FOS) are considered prebiotic compounds and are found in different vegetables and fruits but at low concentrations. FOS are produced by enzymatic transformation of sucrose using fructosyltransferase (FTase). Development of new production methods and search for FTase with high activity and stability for FOS production Is an actual research topic. In this article is discussed the most recent advances on FTase and its applications. Different microorganisms have been tested under various fermentation systems in order to identify and characterize new genes codifying for FTase. Some of these genes have been isolated from bacteria, fungi, and plants, with a wide range of percentages of identity but retaining the eight highly conserved motifs of the hydrolase family 32 glycoside. Therefore, this article presents an overview of the most recent advances on FTase and its applications.
Keywords
- Enzyme production
- Fructooliogosacarides
- Fructosyltransferase
- 1-kestose
- 1-nystose
- 1-β-fructofuranosyl nystose
1. Introduction
At the present time, there is a growing consumer demand for healthier and calorie-controlled foods. For this reason, food industry has developed different alternatives for sweeteners, and among them is the fructooligosaccharides (FOS). Use of these compounds offers multiple health advantages. FOS are fructose oligomers with a terminal glucosyl unit and a general formula of GFn; where typical values of
FOS can be produced by the action of different types of enzymes with transfructosylation activity (i.e., fructosyltransferase—FTase [EC 2.4.1.9] and/or β-fructofuranosidase—FFases [EC 3.2.1.26]). These enzymes are obtained from different plants and microorganisms [4]. The reaction mechanism of FTase depends on enzyme source [5]. Most of these enzymes have been isolated from different fungal strains such as:
2. FTase: an overview
FOS can be synthesized in nature by the catalytic action of enzymes with transfructosylating activity. They are classified as 1F-FTases (E.C. 2.4.1.9, E.C. 2.4.1. 99, and E.C. 2.4.1.100), or β -FFases (, E.C. 3.2.1.26). FTase catalyzes the transfer of a fructosyl group to a molecule of sucrose or a FOS when a FOS with a chain longer by one fructosyl unit is formed [8]. This enzyme also mediates polymerization reactions, where degree of polymerization (DP) decreases to the maximum by transferring fructosyl units from higher molecular mass fructans [9]. The reaction mechanism of the FTases depends on the enzyme source. In plants and some microorganisms, a series of enzymes act together, whereas a single enzyme works in most of the microorganisms [10].
The FTase that converts sucrose to the shortest β (2–1) linked fructan 1-kestose is called sucrose: sucrose 1-FTase (1-SST) [11]. It is reported that, FTase differs in molecular weight and properties depending on its origin [12]. Properties of FTases can change according to the microorganism and culture medium composition, especially the carbon source, which can play a role as an inductor [1]. FTase can be produced intra- and/or extracellular by different microorganisms, including bacteria and fungi. Despite the large number of microbial FTase producers, only some of them have the potential for industrial application and have been used in several studies about FOS production [1]. The transfructosylating activity is responsible for FOS production from sucrose, although quantitative differences exist because of the microbial strains [13].
FTase has been produced using both solid and liquid fermentation, and FOS obtained by these fermentations have been reported. Factors affecting FOS by fermentation were mentioned, such as temperature, pH, and substrate concentration [14, 15]. FTase has a temperature optimum between 50 and 60°C, and the optimal pH is between 4.5 and 6.5 [1, 8].
2.1. Mechanism of action
The reaction mechanism depends on the enzyme source and purity. The accepted mechanism is a type disproportionate reaction where FTase catalyzes the transfer of a fructosyl moiety of a sucrose or fructooligosacharide donor to another sucrose or FOS acceptor to provide a superior FOS [1]. The reaction mechanism has been expressed as follows:
where GF is sucrose or FOS
3. Microbial and plant FTases
Several fungal strains, especially those from
Bacterial strains have been reported to produce different inulinases, but reports on enzymes able to produce FOS are scarce from bacterial strains. Someone bacteria mentioned to produce these enzymes are the following:
The FTases obtained from plants have other amino acid composition that is different from microbial FTases such as sucrose: sucrose 1-FTase (1-SST) and fructan: fructan 1-FTase (1-FFT). Plants such as
4. Structure of FTase
According to the Protein Data Bank (PDB) of Research Collaborators for Structural Bioinformatics (RCSB) data base, the crystal dimensional structure of FTase from
5. FTases properties
5.1. Factors affecting FTase activity
Fructosyltransferase (FTase) participates on FOS/fructan production by catalyzing the transfer of a fructose unit from one sucrose/fructan to another [26]. This enzyme has been included in the glycoside hydrolase family 32 (GH32) and has been isolated from different sources, and the optimal conditions for the enzyme activity have been reported (Table 2). The optimal temperature reported for FTase enzyme activity ranges from 52 to 65°C, while the optimal pH varies widely from 4.5 to 8.0 [27, 28]. There are different reports mentioned about the chemical reagents and amino acids that positively affect FTase activity [29, 30]. On the other hand, there is a controversy in the use of detergents—some authors mention that these compounds enhance FTase activity [29], and in contrast there are others who mention that these compounds negatively affect FTase activity [27].
Source | Temperature | pH | Positive effect | Observation | References |
---|---|---|---|---|---|
52 °C | 4.5 | FeSO4, Fe2+, Fe2+ Ca2+ | Intra- and extracellular | [27] | |
Marine |
65°C | 8.0 | Intracellular | [28] | |
60°C | 5.0–7.0 | Dithiothreitol, 2-mercaptoethanol, sodium dodecylsulphate, Tween 80 |
[29] | ||
55 °C | 5.5 | Leucine induced slightly extracellular production |
Intra- and extracellular | [30, 31] |
5.2. Carbon and nitrogen sources
Different reports mentioned that the preferred carbon source to produce FTase is sucrose. Patil and Butle [31] indicated that
5.3. FTase biochemical properties
Biochemical properties of FTase may change depending on its origin. Ghazi
Chuankhayan
6. FTases gene organization
Genome sequence of different microorganisms and vegetables has allowed identification of some enzymes, development of new products, improvement of strains, and increase of process efficiency. There are some reports of isolation and cloning of the FTase gene. The genes coding for FTase have been isolated from bacteria, fungi, and plants, with a wide range of percentages of identity but retaining the eight highly conserved motifs of hydrolyses family 32 glycoside [35]. Fungal FTase genes have been isolated mainly from
The gene that encodes
7. Fructooligosaccharides
FOS is a common name for fructose oligomers and corresponds to complex carbohydrates which are nondigestible oligosaccharide food ingredients and are fermentable by the gut microbiota. For this reason, they can be classified as prebiotics, and its commercial production has increased in response to a growing consumer demand for the so-called “health foods” [16, 39]. FOS are mainly composed of 1-kestose (GF2), 1-nystose (GF3), and 1- β-fructofuranosyl nystose (GF4), in which 1–3 fructosyl units (F) are bound at the β (2–1) status of sucrose molecule (GF) (Figure 1) [4].
FOS can be found in several vegetal sources such as tomato, onion, barley, garlic, Jerusalem artichoke, banana, rye, honey, sugar beet, to name a few; however, FOS concentration in these sources is low, and mass production are limited by seasonal conditions [3, 4]. At the industrial level, FOS are mainly produced from the disaccharide sucrose by action of different microbial enzymes with transfructosylating activity such as FTase (EC 2.4.1.9) and/or β-fructofuranosidase (EC 3.2.1.26), [4]. Moreover, FOS compounds have received a generally recognized as safe status (GRAS) from the Food and Drug Administration (FDA) and has been consumed because of the several benefits of FOS to human health such as calorie-free and noncariogenic sweeteners, stimulate bifidobacteria growth, and activation of the immune system; have been claimed to contribute to the prevention of colon cancer and reduce the levels of serum cholesterol, phospholipids, and triglycerides; also promote calcium and magnesium absorption in animals and the human gut [14, 19, 22, 40, 41].
Dominguez
7.1. FOS production
Production of FOS has received particular attention in recent years, so there is necessity for the development of new enzymatic systems [42]. FOS represent one of the major classes of bifidogenic oligosaccharides in terms of production volume. Kestose and nystose are the main prebiotic compounds, which can be principally produced by hydrolysis of inulin or by transfructosylation of sucrose [24]. The enzymes that are potentially useful for high production of FOS were reported about three decades ago. Hidaka
8. Use of FTAse for FOS production
FOS have demonstrated important properties for improving human health, thus they have attracted an increased interest mainly as ingredients for food applications. They contribute to 10% of the natural sweeteners, and their demand has risen rapidly (about 15% per year) in the last 15 years [45]. Consequently, establishing sustainable and economically viable industrial process for the production of FOS with high yields and productivities is strongly desirable [46]. These can be manufactured by three methods: (1) extraction from inulin-rich plant materials, (2) by enzymatic synthesis from sucrose, and (3) by enzymatic degradation of inulin [45, 47]. Most of the FOS marketed as food ingredients/nutritional supplements are synthesized either from sucrose by the action of FTases [48, 49] or by enzymatic degradation of inulin [50, 51]. In this section, we will discuss the production of FOS through FTase.
Commercial production of FOS was first developed using enzymatic fructosyl transfer on sucrose by Hidaka
Nowadays, to reduce cost, enzyme immobilization techniques have been applied. Fungal β-fructofuranosidase has been covalently immobilized onto inorganic supports such as porous glass or porous silica [54, 60].
However, it has been observed that enzymes immobilized on a porous support decrease apparently its enzymatic activity because of diffusion resistance. Instead, the use of magnetic nanoparticles is proposed, which offers (a) a higher specific surface area that permits binding of a larger amount of enzyme, (b) relatively low mass transfer resistance and (c) selective separation from a reaction mixture by application of a magnetic field [61, 62]. Chen
Another alternative for FOS production is the use of solid-state fermentation (SSF). Most investigations on FOS production are based on submerged fermentation systems, but SSF is attractive because of low capital cost and low demand of water, generating less wastewater as a consequence. Besides, higher productivities and yields could be obtained at industrial scale [14]. Mussatto
9. Properties of FOS
General structure of FOS can be depicted as GFn, where “
FOSs contain several qualities that make its usage possible as an alternative sweetener in the food market. They are water soluble and one-third as sweet as sucrose [67]. However, their viscosity and thermal stability is higher than sucrose. They are stable in a pH range from 4.0 to 7.0 and can be refrigerated for a period of one year. Their high moisture-retaining capacity provides prevention of excessive drying besides controlling microbial contamination owing their low water interacting activity [68].
They can be considered as noncariogenic sugar substitutes in confectionary, gums, and drinks since they cannot serve as a substrate of
10. FOS as prebiotic
The most widely used definition for prebiotic is “nondigestible food ingredient that beneficially affects host’s health by selectively stimulating the growth and/or activity of one or a limited number of bacteria in the colon” [73]. In 2004, the definition was updated, and it was defined as “selectively fermented ingredients that allow specific changes, both in the composition and/or activity in the gastrointestinal microbiota that confers benefits upon host well-being and health” [74]. According to this, prebiotics are a major part of the functional foods and among them, the FOS are in focus due to their functional properties and economical potential [65, 75].
A prebiotic must fulfill three criteria: (1) no hydrolysis or absorption in the upper part of the digestive system, (2) selective substrate for one or more desired bacteria species in the colon and stimulation of that species regarding growth and activation and (3) able to positively influence the numeric proportion of different bacteria species in the colon [76]. FOS selectively stimulates the growth of
Many Bifidobacteria and
Antiinflammatory and antitumorigenic roles of SCFA have been reported [81, 82]. As a result of the prebiotic function, a decrease in inflammatory markers such as phagocytosis and interleukin (IL)-6 production by increasing CD3+, CD4+, and CD8+ populations has been observed [83]. In case of antitumorigenic roles, especially in the context of colon cancer, the action mechanism is yet unclear [80]. However, it is known that butyrate has an important role on DNA methylation thus modifying gene expression so it may directly enhance cell proliferation of normal cells, but suppress cell proliferation of transformed cells. Furthermore, in the presence of butyrate, apoptosis may be enhanced in transformed cells but inhibited in normal cells [84]. Thus, the regular intake of FOS as a part of diet could help to improve health and over all well-being by providing resistance against the intestinal/extra intestinal pathogens, enhancing the growth of the colon microbiota which have metabolic activities and biochemical processes with a tremendous influence in human host [85].
11. Applications of FOS
FOS are components of functional food that are becoming popular in the society because they have a potential for enhancing flavor quality and physicochemical properties of food products, besides FOS offer various benefits for human health and are also of industrial interest [34]. FOS are used in different food applications and other areas because of its positive impact on human health, physical performance, or state of mind [12], and the most relevant uses in food formulations are the following: beverages (fruit drinks, coffee, cocoa, tea, soda, health drinks, and alcoholic beverages), dairy products (fermented milk, instant powders, powdered milk, and ice cream), also in light jam products and confectionary [86].
12. Functional foods
The growing interest of consumers in the relationship between nutrition and health has increased demand among the population for food products that improve or benefit their health beyond basic nutrition [87, 88]. Because of this demand, both the academic community and the food industry have focused on developing products that meet these characteristics, which are now called functional foods.
The term “functional foods” was first coined in Japan after a group of scientists and nutritionists conducted numerous studies and defined them as “Food for specified health uses” (FoSHU) [89]. Though there is a great number of definitions, Doyon and Labrecque [90] identified four key concepts after reviewing more than 20 definitions: (a) health benefits, (b) the nature of the food, (c) level of function, and (d) consumption pattern. The definition of functional food has evolved, and the latest is that proposed by the European Commission for concerted action Functional Food Science in Europe (FUFOSE) that mentions that “a food can be regarded as ‘functional’ if it is satisfactorily demonstrated to beneficially effect one or more target functions in the body, beyond adequate nutritional effects, in a way that is relevant to either an improved state of health and well-being and/or reduction of risk of disease. Functional foods must remain as food and they must demonstrate their effects in amounts that can normally be expected to be consumed in the diet: they are not pills or capsules, but part of a normal food pattern” [91, 92].
The challenges for the food industry are great so that the biological value of the functional ingredient is not disturbed and sensory characteristics of the food are acceptable [93]. According to various investigations, the success and acceptance of these foods is influenced by factors such as clarity and understanding of the information about nutrition and health benefits that are provided to consumers, especially in elderly consumers [87].
Experts recognize that there are scientific evidence on the effectiveness of various functional foods, which can be useful to balance a poor diet or assist in avoiding health problems in some cases [94]. In general, the consumers’ attitude towards functional foods is positive and have great potential in the food industry.
13. Applications of FOS in food formulations
FOS are ingredients that have been applied in a variety of food matrices, their prebiotic potential has been proven, and its technological properties allow easy incorporation into foods, mainly those that are probiotics [95]. The FOS have comparable glucose syrups and sugar properties and proved approximately a 30–50% sweetness compared with sugar table. Therefore, their application has a dual benefit: (1) as a substitute for sugar and (2) for their prebiotic properties [96].
Akalin and Erisir [97] evaluated the effect of supplementation of oligofructose or inulin in symbiotic ice cream, in the rheological properties and probiotics survival. They found that the survival rate of the probiotics during storage at 30, 40, and 90 days was better with oligofructose. The FOS were evaluated in cookies and Quicks bread and found that consumers had preference equal to or greater for products supplemented with FOS [96, 98]. Although the FOS are easy to incorporate into foods such as yogurt, processing conditions such as acidity and temperature should be considered since they have reported low prebiotic activities under acidic conditions and high thermal processing times [95].
New applications in different food matrices are being evaluated. Valencia
There is an innovative trend in the FOS application in different types of food and, undoubtedly, to maximize the benefits that can confer the FOS, factors as type of food matrix, processing conditions, and added amount should be considered.
14. Future trends
Because of the importance of this enzyme in the modern industry, it is important to relate a set of FTases from different organisms to allow the identification of features that could be used for the identification and classification of new FTases, and also it is necessary to improve the conditions and costs of FTases production process. Further studies of gene sequencing will allow distinguishing among the set of FTase and β FFase enzymes.
15. Conclusions
The studies on production and application of FOS are of high interest for food industry because of several health benefits and biofunctional properties that these compounds provide. FOS can be synthesizing from precursors such as sucrose using FTase enzymes. These enzymes can be obtained from different microorganisms (bacteria and fungi) and plants. The main disadvantage of this production is the low yields of enzymatic activity and FOS. Thus, search for new microbial sources of FTase enzymes is a very important research topic as well as studies about the evolution of FTase genes from different sources, and relate their function with the nucleotide sequence using functional genomics studies.
Acknowledgments
This project was financially supported by the Universidad Autónoma de Coahuila. MRMM would like to thank the financial support received from CONACYT during her master’s degree.
References
- 1.
Maiorano A. E., Piccoli R. M., Da Silva E. S., De Andrade Rodrigues M. F. Microbial production of fructosyltransferases for synthesis of prebiotics. Biotechnology Letters . 2008; 30:1867–1877. DOI:10.1007/s10529-008-9793-3. - 2.
Antošová M., Illeová V., Vandáková M., Družkovská A., Polakovič M. Chromatographic separation and kinetic properties of fructosyltransferase from Aureobasidium pullulans .Journal of Biotechnology , 2008; 135:58–63. DOI:10.1016/j.jbiotec.2008.02.016. - 3.
Mussatto S. I., Prata M. B., Rodrigues L. R., Teixeira J. A. Production of fructooligosaccharides and β-fructofuranosidase by batch and repeated batch fermentation with immobilized cells of Penicillium expansum. European Food Research and Technology . 2012; 235:13–22. DOI:10.1007/s00217-012-1728-5. - 4.
Mussatto S. I., Aguilar C. N., Rodrigues L. R., Teixeira J. A. Colonization of Aspergillus japonicus on synthetic materials and application to the production of fructooligosaccharides.Carbohydrate Research . 2009; 344:795–800. DOI:10.1016/j.carres.2009.01.025. - 5.
Sánchez O. F., Rodriguez A. M., Silva E., Caicedo L. A. Sucrose biotransformation to fructooligosaccharides by Aspergillus sp. N74 Free Cells.Food and Bioprocess Technology . 2008; 3:662–673. DOI:10.1007/s11947-008-0121-7. - 6.
Dominguez A., Nobre C., Rodrigues L. R., Peres A. M., Torres D., Rocha I., Teixeira J. New improved method for fructooligosaccharides production by Aureobasidium pullulans .Carbohydrate Polymers . 2012; 89:1174–1179. DOI:10.1016/j.carbpol.2012.03.091. - 7.
Dominguez A. L., Rodrigues L. R., Lima N. M., Teixeira J. A. An overview of the recent developments on fructooligosaccharide production and applications. Food and Bioprocess Technology . 2013; 7:324–337. DOI:10.1007/s11947-013-1221-6. - 8.
Antošová M., Polakovič M. Fructosyltransferases: the enzymes catalyzing production of fructooligosaccharides. Chemical Papers . 2001; 55:350–358. - 9.
Koops A. J., Jonker H. H. Purification and Characterization of the enzymes of fructan biosynthesis in tubers of Helianthus Fuberbsus Colombia.Plant Physiology . 1996; 110:1167–1175. - 10.
Edelman J., Jefford T. G. The mechanisim of fructosan metabolism in higher plants as exemplified in Helianthus tuberosus .New Phytologist .1968;67:517–531. DOI:10.1111/j.1469-8137.1968.tb05480.x. - 11.
Altenbach D., Rudiño-Pinera E., Olvera C., Boller T., Wiemken A., Ritsema T. An acceptor-substrate binding site determining glycosyl transfer emerges from mutant analysis of a plant vacuolar invertase and a fructosyltransferase. Plant Molecular Biology . 2009; 69:47–56. DOI:10.1007/s11103-008-9404-7. - 12.
Sangeetha P. T., Ramesh M. N., Prapulla S. G. Recent trends in the microbial production, analysis and application of Fructooligosaccharides. Trends in Food Science and Technology . 2005; 16:442–457. DOI:10.1016/j.tifs.2005.05.003 - 13.
Hidaka H., Hirayama M., Sumi N. A Fructooligosaccharide-producing enzyme from. Agricultural and Biological Chemistry . 1988; 52:1181–1187. - 14.
Mussatto S. I., Teixeira J. A. Increase in the fructooligosaccharides yield and productivity by solid-state fermentation with Aspergillus japonicus using agro-industrial residues as support and nutrient source.Biochemical Engineering Journal . 2010; 53:154–157. DOI:10.1016/j.bej.2010.09.012 - 15.
Sangeetha P. T., Ramesh M. N., Prapulla S. G. Production of fructosyl transferase by Aspergillus oryzae CFR 202 in solid-state fermentation using agricultural by-products.Applied Microbiology and Biotechnology . 2004; 65:530–537. DOI:10.1007/s00253-004-1618-2 - 16.
La Rotta C. E., Ospina S. A., López-Munguía A. Production and characterization of crude enzimatic extracts with fructosyl transferase activity. Revista Colombiana de Ciencias Químico-Farmacéuticas . 1998; 27:53–56 (in Spanish). - 17.
Wang X. D., Rakshit S. K. Improved extracellular transferase enzyme production by Aspergillus foetidus for synthesis of isooligosaccharides.Bioprocess Engineering . 1999; 20: 429–434. - 18.
Sangeetha P. T., Ramesh M. N., Prapulla S. G. Production of fructo-oligosaccharides by fructosyl transferase from Aspergillus oryzae CFR 202 andAureobasidium pullulans CFR 77.Process Biochemistry . 2004; 39:755–760. DOI:10.1016/S0032-9592(03)00186-9 - 19.
Sangeetha P. T., Ramesh M. N., Prapulla S. G. Fructooligosaccharide production using fructosyl transferase obtained from recycling culture of Aspergillus oryzae CFR 202.Process Biochemistry . 2005; 40:1085–1088. DOI:10.1016/j.procbio.2004.03.009 - 20.
Sangeetha P. T., Ramesh M. N., Prapulla S. G. Maximization of fructooligosaccharide production by two stage continuous process and its scale up. Journal of Food Engineering . 2005; 68:57–64. DOI:10.1016/j.jfoodeng.2004.05.022. - 21.
MasahiroKurakake, OgawaKenji, SugieMotoki, A. T., Kouji Sugiura, T. Komaki. Two types of fructofuranosidases from Aspergillus oryzae KB.Journal of Agricultural and Food Chemistry . 2008; 56:591–596. - 22.
Sathish T., Prakasham R. S. Intensification of fructosyltransferases and fructo-oligosaccharides production in solid state fermentation by Aspergillus awamori GHRTS.Indian Journal of Microbiology . 2013; 53:337–342. DOI:10.1007/s12088-013-0380-5. - 23.
Yang H., Wang Y., Zhang L., Shen W. Heterologous expression and enzymatic characterization of fructosyltransferase from Aspergillus niger inPichia pastoris .New Biotechnology . 2015; 00:1–7. DOI:10.1016/j.nbt.2015.04.005. - 24.
Yoshikawa J., Amachi S., Shinoyama H., Fujii T. Multiple β-fructofuranosidases by Aureobasidium pullulans DSM2404 and their roles in fructooligosaccharide production.FEMS Microbiology Letters . 2006; 265:159–163. DOI:10.1111/j.1574-6968.2006.00488.x - 25.
Sprenger N., Bortlik K., Brandt A., Boller T., Wiemken A. Purification, cloning, and functional expression of sucrose: fructan 6-fructosyltransferase, a key enzyme of fructan synthesis in barley. Proceedings of the National Academy of Sciences . 1995; 92:11652–11656. - 26.
Chuankhayan P., Hsieh C. Y., Huang Y. C., Hsieh Y. Y., Guan H. H., Hsieh Y. C., Chen C. J. Crystal structures of Aspergillus japonicus fructosyltransferase complex with donor/acceptor substrates reveal complete subsites in the active site for catalysis.Journal of Biological Chemistry . 2010; 285:23251–23264. DOI:10.1074/jbc.M110.113027. - 27.
ArtheeR., VijilaK. Study on fructosyltransferase enzyme from Aspergillus sp. in fructooligosaccharides production. Research Journal of Recent Sciences. 2014; 3:147–153. - 28.
AmrendraKumar, Vaishnavi .R, Saravanakumar .,A K. S.A. and, Tank S. K. Biotransformation of sucrose by using thermostable and alkaline fructosyltransferase enzyme isolated. International Journal of Science, Environment . 2014; 3:708–713. - 29.
Ghazi I., Fernandez-Arrojo L., Garcia-Arellano H., Ferrer M., Ballesteros A., Plou F. J. Purification and kinetic characterization of a fructosyltransferase from Aspergillus aculeatus .Journal of Biotechnology . 2007; 128:204–211. DOI:10.1016/j.jbiotec.2006.09.017. - 30.
Dhake,A. B., Patil M. B. Effect of substrate feeding on production of fructosyltransferase by Penicillium purpurogenum .Brazilian Journal of Microbiology . 2007; 38:194–199. DOI:10.1590/S1517-83822007000200002. - 31.
Patil M. B., ButleA.. Fructosyltransferase production by indigenously isolated Syncephalastrum racemosum Cohn.Journal of Global Biosciences . 2014; 3:597–603. - 32.
Tamura K. I., Kawakami A., Sanada Y., Tase K., Komatsu T., Yoshida M. Cloning and functional analysis of a fructosyltransferase cDNA for synthesis of highly polymerized levans in timothy ( Phleum pratense L.).Journal of Experimental Botany . 2009; 60:893–905. DOI:10.1093/jxb/ern337. - 33.
Van Hijum S. a F. T., Van Geel-Schutten G. H., Rahaoui H. Van der Maarel M. J. E. C., Dijkhuizen, L. Characterization of a novel fructosyltransferase from Lactobacillus reuteri that synthesizes high-molecular-weight inulin and inulin oligosaccharides.Applied and Environmental Microbiology . 2002; 68:4390–4398. DOI:10.1128/AEM.68.9.4390-4398.2002. - 34.
Rehm J., Willmitzer L., Heyer A. G. Production of 1-kestose in transgenic yeast expressing a fructosyltransferase from Aspergillus foetidus .Journal of Bacteriology . 1998; 180:1305–1310. - 35.
Rodríguez M. A, Sánchez O. F., Alméciga-Díaz C. J. Gene cloning and enzyme structure modeling of the Aspergillus oryzae N74 fructosyltransferase.Molecular Biology Reports . 2011; 38:1151–1161. DOI:10.1007/s11033-010-0213-0. - 36.
Goosen C., Yuan X.-L., van Munster J. M., Ram A. F. J., van der Maarel M. J. E. C., Dijkhuizen L. Molecular and biochemical characterization of a novel intracellular invertase from Aspergillus niger with transfructosylating activity.Eukaryotic Cell . 2007; 6: 674–681. DOI:10.1128/EC.00361-06. - 37.
Alméciga-Díaz C. J., Gutierrez Á. M., Bahamon I., Rodríguez A., Rodríguez M. A, Sánchez O. F. Computational analysis of the fructosyltransferase enzymes in plants, fungi and bacteria. Gene . 2011; 484:26–34. DOI:10.1016/j.gene.2011.05.024. - 38.
Heyer A. G., Wendenburg R. Gene cloning and functional characterization by heterologous expression of the fructosyltransferase of Aspergillus sydowi IAM 2544.Applied and Environmental Microbiology . 2001; 67:363–370. DOI:10.1128/AEM.67.1.363. - 39.
Chien C.-S., Lee W.-C., Lin T.-J. Immobilization of Aspergillus japonicus by entrapping cells in gluten for production of fructooligosaccharides. Enzyme and Microbial Technology . 2001; 29:252–257. DOI:10.1016/S0141-0229(01)00384-2. - 40.
Mussatto S. I., Ballesteros L. F., Martins S., Maltos D. A. F., Aguilar C. N., Teixeira J. A. Maximization of fructooligosaccharides and β-fructofuranosidase production by Aspergillus japonicus under solid-state fermentation conditions.Food and Bioprocess Technology . 2013; 6:2128–2134. DOI:10.1007/s11947-012-0873-y. - 41.
Silva J. B. Da, Fai A. E. C., dos Santos R., Basso L. C., Pastore G. M. Parameters evaluation of fructooligosaccharides production by sucrose biotransformation using an osmophilic Aureobasium pullulans strain.Procedia Food Science . 2011; 1:1547–1552. DOI:10.1016/j.profoo.2011.09.229. - 42.
L’Hocine, L., Wang Z., Jiang B., Xu S. Purification and partial characterization of fructosyltransferase and invertase from Aspergillus niger AS0023.Journal of Biotechnology . 2000; 81:73–84. DOI:10.1016/S0168-1656(00)00277-7. - 43.
McCleary B. V., Gibson T. S., Sheehan H., Casey A., Horgan L., O’Flaherty, J. Purification, properties, and industrial significance of transglucosidase from Aspergillus niger .Carbohydrate Research . 1989; 185:147–162. - 44.
Antosova M., Polakovic M., Slovinská M., Madlová A., Illeová V., Bales V. Effect of sucrose concentration and cultivation time on batch production of fructosyltransferase by Aureobasidium pullulans CCY 27-1-1194.Hemical Papers-Slovak Academy of Sciences . 2003; 56:394–399. - 45.
Panesar P.S., Bali V., Kumari S., Babbar N., Oberoi H.S. Prebiotics. In: G.S. Brar (Ed.), Biotransformation of Waste Biomass into High Value Biochemicals. Springer. Ney York, USA, 2014; 504 pp. - 46.
Mussatto S. I., Aguiar L. M., Marinha M. I., Jorge R. C., Ferreira E. C. Economic analysis and environmental impact assessment of three different fermentation processes for fructooligosaccharides production. Bioresource Technology . 2015; 198:673–681. DOI:10.1016/j.biortech.2015.09.060. - 47.
Rastall R.A. Functional oligosaccharides: application and manufacture. Annual Review of Food Science and Technology . 2010; 1:305–339. - 48.
Bali V., Panesar P.S., Bera M.B., Panesar R. Fructo-oligosaccharides: production, purification and potential applications. Critical Reviews in Food Science and Nutrition . 2015; 55:1475–1490. - 49.
Ganaie M. A., Rawat H. K., Wani O. A., Gupta U. S., Kango N. Immobilization of fructosyltransferase by chitosan and alginate for efficient production of fructooligosaccharides. Process Biochemistry . 2014; 49:840–844. DOI:10.1016/j.procbio.2014.01.026. - 50.
Mutanda T., Mokoena M. P., Olaniran, A. O., Wilhelmi, B. S., Whiteley, C. G. Microbial enzymatic production and applications of short-chain fructooligosaccharides and inulooligosaccharides: Recent advances and current perspectives. Journal of Industrial Microbiology and Biotechnology . 2014; 41:893–906. DOI:10.1007/s10295-014-1452-1. - 51.
Singh R. S., Singh R. P. Production of fructooligosaccharides from inulin by endoinulinases and their prebiotic potential. Food Technology and Biotechnology . 2010; 48: 435–450. - 52.
Hidaka,H., Eida,T., Tokunaga,T., Tashiro,Y. Effects of fructooligosaccharides on intestinal flora and human health. Bifidobacteria and Microflora . 1986; 5:37–50. - 53.
Nguyen,Q.D., Rezessy-Szabo,J.M., Bhat,M.K. Purification and some properties of b-fructofuranosidase from Aspergillus niger IMI303386.Process Biochemistry . 2005; 40:2461–2466. - 54.
Hayashi,S., Matsuzaki,K., Takasaki,Y., Ueno,H., Imada,K. Production of b-fructofuranosidase by Aspergillus japonicus .World Journal of Microbiology and Biotechnology . 1992; 8:155–159. - 55.
Mussatto,S.I., Aguilar,C.N., Rodrigues,L.R., Teixeira,J.A. Fructooligosaccharides and b-fructofuranosidase production by Aspergillus japonicus immobilized on lignocellulosic materials.Journal of Molecular Catalisis B: Enzymatic . 2009; 59:76–81. - 56.
Chang,C.T., Lin,Y.Y., Tang,M.S., Lin,C.F. Purification and properties of betafructofuranosidase from Aspergillus oryzae ATCC 76080.Biochemistry and Molecular Biology International . 1994; 32:269–277. - 57.
Jung,K.H., Lim,J.Y., Yoo,S.J., Lee,J.H., Yoo,M.Y. Production of fructosyltransferase from Aureobasidium pullulans .Biotechnology Letters . 1987; 9:703–708. - 58.
Yoshikawa,J., Amachi,S., Shinoyama,H., Fujii,T. Purification and some properties of b-fructofuranosidase I formed by Aureobasidium pullulans DSM 2404.Journal Bioscience and Bioengineering . 2007; 103:491–493. - 59.
Nishizawa,M., Maruyama,Y., Nakamura,M. Purification and characterization of invertase isozyme from Fusarium oxysporum .Agricultural and Biological Chemistry . 1980; 44:489–498. - 60.
Ortega-Muñoz,M., Morales-Sanfrutos,J., Megia-Fernandez,F., Lopez-Jaramillo,F. J., Hernandez-Mateo,F., Santoyo-Gonzalez,F. Vinyl sulfone functionalized silica: a ready to use pre-activated material for immobilization of biomolecules. Journal of Materials Chemistry . 2010; 20:7189–7196. - 61.
Halling,P.J., Dunnill,P. Magnetic supports for immobilized enzymes and bioaffinity adsorbents. Enzyme and Microbial Technology. 1980; 2: 2–10. - 62.
Kim,J., Grate,J.W., Wang,P. Nanostructures for enzyme stabilization. Chemical Engineering Science . 2006; 61:1017–1026. - 63.
Chen S. C., Sheu D. C., Duan K. J. Production of fructooligosaccharides using β-fructofuranosidase immobilized onto chitosan-coated magnetic nanoparticles. Journal of the Taiwan Institute of Chemical Engineers . 2014; 45:1105–1110. DOI:10.1016/j.jtice.2013.10.003. - 64.
Duan,K. J., Chen,J.S., Sheu,D.C. Kinetic studies and mathematical model for enzymatic production of fructooligosaccharides from sucrose . Enzyme and Microbial Technology . 1994; 16:334–339. - 65.
Yun J. W. Fructooligosaccharides—occurrence, preparation, and application. Enzyme and Microbial Technology . 1996; 19:107–117. DOI:10.1016/0141-0229(95)00188-3. - 66.
Meyer D., Stasse-Wolthuis M. The bifidogenic effect of inulin and oligofructose and its consequences for gut health. European Journal of Clinical Nutrition , 63:1277–1289. DOI:10.1038/ejcn.2009.64. - 67.
Salinas M. A., Perotti N. A. Production of fructosyltransferase by Aureobasidium sp. ATCC 20524 in batch and two-step batch cultures.Journal of India Industrial Microbiology Biotechnology . 2009; 36:39–43. - 68.
Crittenden R. G., Playne M. J. Production, properties and applications of food-grade oligosaccharides. Trends in Food Science and Technology . 1996; 7: 353–361. - 69.
Oku T. Special physiological functions of newly developed mono-and oligosaccharides. In: Goldberg (Ed.), Functional Foods: Designer Foods, Pharmafoods, Nutraceuticals. Chapman &Hall, Ney York, USA . pp. 202–218. - 70.
Kaur N., Gupta A. K. Applications of inulin and oligofructose in health and nutrition. Journal of Biosciences . 2002; 27:703–714. DOI:10.1007/BF02708379. - 71.
Rycroft C. E., Jones M. R., Gibson G. R., Rastall R. A. A comparative in vitro evaluation of the fermentation properties of prebiotic oligosaccharides. Journal of Applied Microbiology . 2001; 91:878–887. DOI:10.1046/j.1365-2672.2001.01446.x. - 72.
Villegas B., Costell E. Flow behaviour of inulin-milk beverages. Influence of inulin average chain length and of milk fat content. International Dairy Journal . 2007; 17:776–781. DOI:10.1016/j.idairyj.2006.09.007. - 73.
Gibson,G. R., Roberfroid,M. B. Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. Journal of Nutrition . 1995; 125:1401–1412. - 74.
Gibson G. R., Probert, H. M., Loo, J. Van, Rastall R. A, Roberfroid M. B. Dietary modulation of the human colonic microbiota: updating the concept of prebiotics. Nutrition Research Reviews . 2004; 17:259–275. DOI:10.1079/NRR200479. - 75.
Flores-Gallegos A. C., Contreras-Esquivel J. C., Morlett-Chavez J. A, Aguilar C. N., Rodriguez-Herrera R. Comparative study of fungal strains for thermostable inulinase production. Journal of Bioscience and Bioengineering . 2015; 119:421–426. DOI:10.1016/j.jbiosc.2014.09.020. - 76.
Kovács Z., Benjamins E., Grau K., Rehman A.U., Ebrahimi M., and Czermak P. Recent developments in manufacturing oligosaccharides with prebiotic functions. Advances in Biochemical Engineering Biotechnology . 2014; 143:257–295. - 77.
Scholz-Ahrens K.E., Ade P., Marten B., Weber P., Timm W., Asil Y., Glüer C., Schrezenmeir J. Mint: Prebiotics, probiotics, and synbiotics affect mineral absorption, bone mineral content and bone structure. Journal Nutrition . 2007; 137:838S–8346S. - 78.
Tazoe H., Otomo Y., Kaji I., Tanaka R., Karaki S.I., Kuwahara A. Roles of short-chain fatty acids receptors, GPR41 and GPR43 on colonic functions. Journal of Physiology and Pharmacology . 2008; 59:251–262. - 79.
Sangeetha P. T., Ramesh M. N., Prapulla S. G. Microbial production of fructooligosaccharides. Asian Journal of Microbiology Biotechnology Environmental Sciences . 2003; 5:313–331. - 80.
Pool-Zobel B.L., Neudecker C., Domizlaff I., Ji S., Schillinger U., Rumney C., Moretti M., Vilarini I., Scassellati S.R., Rowland I. Lactobacillus - andBifidobacterium -mediated antigenotoxicity in the colon of rats.Nutrition and Cancer . 1996; 26:365–380. - 81.
Alva-Murillo N., Ochoa-Zarzosa A., Lopez-Meza J.E. Short chain fatty acids (propionic and hexanoic) decrease Staphylococcus aureus internalization into bovine mammary epithelial cells and modulate antimicrobial peptide expression.Veterinary Microbiology . 2012; 155:324–331. - 82.
Tan J., Mckenzie C., Potamitis M., Thorburn A. N., Mackey C. R., Macia L. The role of short-chain fatty acids in health and disease. Advances in Immunology . 2014; 121:91–119. - 83.
Guigoz Y., Rochat F., Perruisseau-Carrier G., Rochat I., Schiffrin E. J. Effects of oligosaccharide on the faecal flora and non-specific immune system in elderly people. Nutrition Research . 2002; 22:13–25. DOI:10.1016/S0271-5317(01)00354-2. - 84.
Hass R., Busche R., Luciano L., Reale E., Engelhardt W. Lack of butyrate is associated with induction of bax and subsequent apoptosis in the proximal colon of guinea pig. Gastroenterology . 1997; 112:875–881. - 85.
Peshev D., den Ende W. V. Fructans: prebiotics and immunomodulators. Journal of Functional Foods . 2014; 8:348–357. - 86.
Mussatto S. I., Mancilha I. M. Non-digestible oligosaccharides: a review. Carbohydrate Polymers . 2007; 68:587–597. DOI:10.1016/j.carbpol.2006.12.011. - 87.
Vella M.N.; Stratton L.M.; Sheeshka J.; Duncan A.M. Functional food awareness and perceptions in relation to information sources in older adults. Nutrition Journal . 2014; 13:1–25. - 88.
Abdel-Salam A.M. Functional food: hopefulness to good health. American Journal of Food Technology . 2010; 5:86–99. - 89.
Shimizu M. Functional food in Japan: current status and future of gut-modulating food. Journal of Food and Drug Analysis . 2012; 20:213–216. - 90.
Doyon M.; Labrecque J. A. Functional foods: a conceptual definition. British Food Journal . 2008; 110:1133–1149. - 91.
Diplock A., Aggett P., Ashwell M., Bornet F., Fern E., Roberfroid M. Scientific concepts of functional foods in Europe: consensus document. British Journal of Nutrition . 1999; 9:1–27. - 92.
Ozen A. E., Pons A., Tur J. A. Worldwide consumption of functional foods: A systematic review. Nutrition Reviews . 2012; 70:472–481. - 93.
Spence J. T. Challenges related to the composition of functional foods. Journal of Food Composition and Analysis. 2006;19 :S4–S6. - 94.
Crowe K. M., Francis C. Position of the academy of nutrition and dietetics: functional foods. Journal of the Academy of Nutrition and Dietetics . 2013; 113:1096–1103. - 95.
Vega R., Zuniga-Hansen M. E. The effect of processing conditions on the stability of fructooligosaccharides in acidic food products. Food Chemistry . 2015; 173:784–789. - 96.
Handa C., Goomer S., Siddhu A. Physicochemical properties and sensory evaluation of fructoligosaccharide enriched cookies. Journal of Food Science And Technology . 2012; 49:192–199. - 97.
Akalın A. S., Erişir D. Effects of inulin and oligofructose on the rheological characteristics and probiotic culture survival in low fat probiotic Ice cream. Journal of Food Science . 2008; 73:M184-M188. - 98.
Rößle C., Ktenioudaki A., Gallagher E. Inulin and oligofructose as fat and sugar substitutes in quick breads (scones): a mixture design approach. European Food Research and Technology. 2011; 233:167–181. - 99.
Valencia M.S., Salgado S.M., Andrade S.A.C., Padilha V.M., Livera A.V.S., Stamford T.L.M. Development of creamy milk chocolate dessert added with fructooligosaccharide and Lactobacillus paracasei subsp.Paracasei LBC 81. LWT––Food Science and Technology . 2016; 69:104–109. - 100.
Resconi V.C., Keenan D.F., Barahona M., Guerrero L., Kerry J.P., Hamill R.M. Rice starch and fructo-oligosaccharides as substitutes for phosphate and dextrose in whole muscle cooked hams: sensory analysis and consumer preferences. LWT—Food Science and Technology. 2016; 66:284–292.