Abstract
Fructosyltransferase (FTase) catalyzes the transfer of a fructosyl group to a sucrose molecule or a fructooligosaccharide (FOS) when a FOS with a longer chain is formed. Production of FTase by two Aspergillus species and its mixture was exploited using solid-state fermentation (SSF) and employing agave sap as substrate. The maximum FTase activity (1.59 U/mL) by Aspergillus oryzae was obtained after 24 h, using a temperature of 30 °C, with an inoculum of 2 × 107 spores/mL. The nucleotide sequence coding for the fructosyltransferase showed 1494 bp and encodes for a protein of 498 amino acids. The hypothetical molecular tertiary structure of Aspergillus oryzae BM-DIA FTase showed the presence of structural domains, such as a five-bladed beta-propeller domain characteristic of GH (glycoside hydrolase) and C terminal, which forms a beta-sandwich module. This study contributes to the knowledge of stability, compatibility, and genetic expression of Aspergillus oryzae BM-DIA under SSF bioprocess conditions for industrial production of fructosyltransferase.
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References
Alméciga-Díaz CJ, Gutierrez AM, Bahamon I, Rodríguez A, Rodríguez MA, Sánchez OF (2011) Computational analysis of the fructosyltransferase enzymes in plants, fungi and bacteria. Gene 484:26–34. https://doi.org/10.1016/j.gene.2011.05.024
Antošová M, Polakovič M (2001) Fructosyltransferases: the enzymes catalyzing production of fructooligosaccharides. Chem Pap 55:350–358
Barth, G., Gallardin, C. (1996): Yarrowia lipolytica. In: Non-Conventional Yeasts in Biotechnology, a Handbook, (K. Wolf ed), Pp. 313-388, Springer-Verlag, Berlin, Germany.
Blix G (1948) The determination of hexosamines according to elson and morgan. Acta Chem Scand 2:467–473
Dominguez A, Nobre C, Rodrigues LR, Peres AM, Torres D, Rocha I, Lima N, Teixeira J (2012) New improved method for fructooligosaccharides production by Aureobasidium pullulans. Carbohydr Polym 89:1174–1179. https://doi.org/10.1016/j.carbpol.2012.03.091
Flores-Gallegos AC, Contreras-Esquivel JC, Morlett-Chávez JA, Aguilar CN, Rodríguez-Herrera R (2015) Comparative study of fungal strains for thermostable inulinase production. J Biosci Bioeng 119:421–426. https://doi.org/10.1016/j.jbiosc.2014.09.020
Flores-Gallegos AC, Morlett-Chávez JA, Aguilar CN, Riutort M, Rodríguez-Herrera R (2014) Gene encoding inulinase isolated from Penicillium citrinum ESS and its molecular phylogeny. Appl Biochem Biotech 175:1358–1370. https://doi.org/10.1007/s12010-014-1280-9
Flores-Maltos DA, Mussatto SI, Contreras-Esquivel JC, Rodríguez-Herrera R, Teixeira JA, Aguilar CN (2016) Biotechnological production and application of fructooligosaccharides. Crit Rev Biotechnol 36:259–267. https://doi.org/10.3109/07388551.2014.953443
Flores-Maltos A, Mussatto SI, Contreras-Esquivel JC, Rodríguez R, Teixeira JA, Aguilar CN (2019) Production of a transfructosylating enzymatic activity associated to fructooligosaccharides. In: Parameswaran B, Varjani S, Raveendran S (eds) Green Bio-processes, 1st edn. Springer, Singapore, pp 345–355
Guan L, Liping C, Yongsen C, Nu Z, Han Y (2017) Expression and activity analysis of fructosyltransferase from Aspergillus oryzae. Protein J 36:352–360. https://doi.org/10.1007/s10930-017-9725-y
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321. https://doi.org/10.1093/sysbio/syq010
Han Y, Liu G, Huang D, Qiao B, Chen L, Guan L, Mao D (2011) Study on the synthesis of sucrose-6-acetate catalyzed by fructosyltransferase from Aspergillus oryzae. New Biotech 28:14–18. https://doi.org/10.1016/j.nbt.2010.07.007
Heyer AG, Wendenburg R (2001) Gene cloning and functional characterization by heterologous expression of the fructosyltransferase of Aspergillus sydowi IAM 2544. Appl Environ Microbiol 67:363–370. http:// dx.doi.org/https://doi.org/10.1128/AEM.67.1.363-370.2001
Huang MP, Wu M, Xu QS, Mo DJ, Feng JX (2016) Highly efficient synthesis of fructooligosaccharides by extracellular fructooligosaccharide-producing enzymes and immobilized cells of Aspergillus aculeatus M105 and purification and biochemical characterization of a fructosyltransferase from the fungus. J Agric Food Chem 64:6425–6432. https://doi.org/10.1021/acs.jafc.6b02115
Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755. https://doi.org/10.1093/bioinformatics/17.8.754
Enríquez-Salazar MI, Veana F, Aguilar CN, De la Garza-Rodríguez IM, López MG, Rutiaga-Quiñones OM, Morlett-Chávez JA, Rodríguez-Herrera R (2017) Microbial diversity and biochemical profile of aguamiel collected from Agave salmiana and A. atrovirens during different seasons of year. Food Sci Biotechnol 26:1003–1011. https://doi.org/10.1007/s10068-017-0141-z
Kurakake M, Ogawa K, Sugie M, Takemura A, Komaki T, Sugiura K (2008) Two types of β-fructofuranosidases from Aspergillus oryzae KB. J Agric Food Chem 56:591–596. https://doi.org/10.1021/jf072762k
Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van Den Ende W (2009) Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. J Exp Bot 60:727–740. https://doi.org/10.1093/jxb/ern333
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lira de Oliveira R, da Silva MF, Converti A, Souza Porta T (2019) Biochemical characterization and kinetic/thermodynamic study of Aspergillus tamarii URM4634 β-fructofuranosidase with transfructosylating activity. Biotechnol Prog 35: 1–12. https://doi.org/10.1002/btpr.2879
Maiorano AE, Moniz-Piccoli R, Sabino-Da-Silva E, De-Andrade-Rodrigues MF (2008) Microbial production of fructosyltransferases for synthesis of pre-biotics. Biotechnol Lett 30:1867–1877. https://doi.org/10.1007/s10529-008-9793-3
Mellado-Mojica E, López MG (2015) Identification, classification, and discrimination of Agave syrups from natural sweeteners by infrared spectroscopy and HPAEC-PAD. Food Chem 167:349–357. https://doi.org/10.1016/j.foodchem.2014.06.111
Muñiz-Márquez DB, Contreras JC, Rodríguez-Herrera R, Mussatto SI, Wong-Paz JE, Teixeira JA, Aguilar CN (2015) Influence of thermal effect on sugars composition of Mexican Agave syrup. CyTA J Food 13:607–612. https://doi.org/10.1080/19476337.2015.1028452
Muñiz-Márquez DB, Contreras JC, Rodríguez R, Mussatto SI, Teixeira JA, Aguilar CN (2016) Enhancement of fructosyltransferase and fructooligosaccharides production by A. oryzae DIA-MF in solid-state fermentation using aguamiel as culture medium. Bioresource Technol 213:276–282. https://doi.org/10.1016/j.biortech.2016.03.022
Muñiz-Márquez DB, Teixeira JA, Mussatto SI, Contreras-Esquivel JC, Rodríguez-Herrera R, Aguilar CN (2019) Fructo-oligosaccharides (FOS) production by fungal submerged culture using aguamiel as a low-cost by-product. LWT 102:75–79. https://doi.org/10.1016/j.lwt.2018.12.020
Mussatto SI, Aguilar CN, Rodrigues LR, Teixeira JA (2009) Colonization of Aspergillus japonicus on synthetic materials and application to the production of fructooligosaccharides. Carbohydr Res 344:795–800. https://doi.org/10.1016/j.carres.2009.01.025
Mussatto SI, Ballesteros LF, Martins S, Flores-Maltos DA, Aguilar CN, Teixeira JA (2013) Maximization of fructooligosaccharides and β-fructofuranosidase production by Aspergillus japonicus under solid-state fermentation conditions. Food Bioprocess Technol 6:2128–2134. https://doi.org/10.1007/s11947-012-0873-y
Mussatto SI, Teixeira JA (2010) Increase in the fructooligosaccharides yield and productivity by solid-state fermentation with Aspergillus japonicus using agro-industrial residues as support and nutrient source. Biochem Eng J 53:154–157. https://doi.org/10.1016/j.bej.2010.09.012
Picazo B, Flores-Gallegos AC, Muñiz-Márquez DB, Flores-Maltos A, Michel-Michel MR de la Rosa O, Rodríguez-Jasso RM, Rodríguez-Herrera R, Aguilar CN (2019) Enzymes for fructooligosaccharides production: achievements and opportunities. In M. Kuddus (ed) Enzymes in Food Biotechnology, 1st edn. Elsevier, pp 303–320.
Rodríguez MA, Sánchez OF, Alméciga-Díaz CJ (2011) Gene cloning and enzyme structure modeling of the Aspergillus oryzae N74 fructosyltransferase. Mol Biol Rep 38:1151–1161. https://doi.org/10.1007/s11033-010-0213-0
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Sangeetha PT, Ramesh MN, Prapulla SG (2004) Production of fructosyl transferase by Aspergillus oryzae CFR 202 in solid-state fermentation using agricultural by-products. Appl Microbiol Biotechnol 65:530–537. https://doi.org/10.1007/s00253-004-1618-2
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739. https://doi.org/10.1093/molbev/msr121
Thadikamala S, Reddy Shetty P (2013) Intensification of fructosyltransferases and fructo-oligosaccharides production in solid state fermentation by Aspergillus awamori GHRTS. Indian J Microbiol 53(3):337–342. https://doi.org/10.1007/s12088-013-0380-5
Velázquez-Hernández ML, Baizabal-Aguirre VM, Bravo-Patiño A, Cajero-Juárez M, Chávez-Moctezuma MP, Valdez-Alarcón JJ (2009) Microbial fructosyltransferases and the role of fructans. J Appl Microbiol 106:1763–1778. https://doi.org/10.1111/j.1365-2672.2008.04120.x
Viniegra-González G, Favela-Torres E, Aguilar CN, De Jesus R-G, Díaz-Godínez G, Augur C (2003) Advantages of fungal enzyme production in solid state over liquid fermentation systems. Biochem Eng J 13:157–167. https://doi.org/10.1016/S1369-703X(02)00128-6
Whelan S, de Bakker PIW, Goldman N (2003) Pandit: a database of protein and associated nucleotide domains with inferred trees. Bioinformatics 19:1556–1563. https://doi.org/10.1093/bioinformatics/btg188
Yang J, Zhang Y (2015) I-TASSER Server: new development for protein structure and function predictions. Nucleic Acids Res 43(W1):W174-181. https://doi.org/10.1093/nar/gkv342
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The authors were financially supported by the National Council for Science and Technology (CONACYT) of Mexico. Author M.R. Michel was financially supported by CONACYT for her MSc studies.
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Michel, M.R., Gallegos, A.C.F., Villarreal-Morales, S.L. et al. Fructosyltransferase production by Aspergillus oryzae BM-DIA using solid-state fermentation and the properties of its nucleotide and protein sequences. Folia Microbiol 66, 469–481 (2021). https://doi.org/10.1007/s12223-021-00862-4
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DOI: https://doi.org/10.1007/s12223-021-00862-4