Production, purification, characterization, and applications of α-galactosidase from Bacillus flexus JS27 isolated from Manikaran hot springs

References

• Goulas, T.; Goulas, A.; Tzortzis, G.; Gibson, G. R. A Novel α-Galactosidase from Βifidobacterium bifidum with Transgalactosylating Properties: Gene Molecular Cloning and Heterologous Expression. Appl. Microbiol. Biotechnol. 2009, 82, 471–477. DOI: 10.1007/s00253-008-1750-5.
   PubMed Web of Science ®Google Scholar
• Omar, R. M.; Galala, A. A.; Badria, F. Medicinal Plants: Dual Source of Enzymes and Enzyme Modulators. Polymorphism 2019, 27, 3.
   Google Scholar
• Bhatia, S.; Singh, A.; Batra, N.; Singh, J. Microbial Production and Biotechnological Applications of α-Galactosidase. Int. J. Biol. Macromol. 2020, 150, 1294–1313.
   PubMedGoogle Scholar
• Álvarez-Cao, M. E.; Becerra, M.; González-Siso, M. I. Biovalorization of Cheese Whey and Molasses Wastes to Galactosidases by Recombinant Yeasts. In Biovalorisation of Wastes to Renewable Chemicals and Biofuels; Rathinam, N. K., Sani, R., Eds.; Elsevier, USA, 2020; pp. 149–161.
   Google Scholar
• Zhang, J.; Song, G.; Mei, Y.; Li, R.; Zhang, H.; Liu, Y. Present Status on Removal of Raff Inose Family Oligosaccharides–A Review. Czech J. Food Sci. 2019, 37, 141–154. DOI: 10.17221/472/2016-CJFS.
   Google Scholar
• Torres, D. P.; Gonçalves, M. D.; Teixeira, J. A.; Rodrigues, L. R. Galacto‐Oligosaccharides: production, Properties, Applications, and Significance as Prebiotics. Compr. Rev. Food Sci. Food Saf. 2010, 9, 438–454.
   PubMed Web of Science ®Google Scholar
• Linares, N. C.; Dilokpimol, A.; Stålbrand, H.; Mäkelä, M. R.; de Vries, R. P. Recombinant Production and Characterization of Six Novel GH27 and GH36 α-Galactosidases from Penicillium subrubescens and Their Synergism with a Commercial Mannanase during the Hydrolysis of Lignocellulosic Biomass. Bioresource Technol. 2020, 295, 122258. DOI: 10.1016/j.biortech.2019.122258.
   PubMedGoogle Scholar
• Chen, S. C.; Wu, S. P.; Chang, Y. Y.; Hwang, T. S.; Lee, T. H.; Hsu, C. H. Crystal Structure of α-Galactosidase from Thermus thermophilus: Insight into Hexamer Assembly and Substrate Specificity. J. Agric. Food Chem. 2020, 68, 6161–6169. DOI: 10.1021/acs.jafc.0c00871.
   PubMedGoogle Scholar
• Singh, R.; Kumar, M.; Mittal, A.; Mehta, P. K. Microbial Enzymes: Industrial Progress in 21st Century. 3 Biotech. 2016, 6, 1–5. DOI: 10.1007/s13205-016-0485-8.
   PubMedGoogle Scholar
• Wang, S.; Hou, W.; Dong, H.; Jiang, H.; Huang, L.; Wu, G.; Zhang, C.; Song, Z.; Zhang, Y.; Ren, H.; et al. Control of Temperature on Microbial Community Structure in Hot Springs of the Tibetan Plateau. PLOS One 2013, 8, e62901. DOI: 10.1371/journal.pone.0062901.
   PubMed Web of Science ®Google Scholar
• Liebl, W.; Wagner, B.; Schellhase, J. Properties of an α-Galactosidase, and Structure of Its Gene galA, within an α-and β-Galactoside Utilization Gene Cluster of the Hyperthermophilic Bacterium Thermotoga maritima. Syst. Appl. Microbiol. 1998, 21, 1–1.
   PubMed Web of Science ®Google Scholar
• Obeidat, M.; Khyami-Horani, H.; Al-Zoubi, A.; Otri, I. Isolation, Characterization, and Hydrolytic Activities of Geobacillus Species from Jordanian Hot Springs. Afr. J. Biotechnol. 2012, 11, 6763–6768.
   Google Scholar
• Chen, M. Y.; Lin, G. H.; Lin, Y. T.; Tsay, S. S. Meiothermus taiwanensis sp. nov., a Novel Filamentous, Thermophilic Species Isolated in Taiwan. Int. J. Syst. Evol. Micr. 2002, 52, 1647–1654.
   PubMedGoogle Scholar
• Courtois, J. E.; Petek, F. α-Galactosidase from Coffee Beans. In Methods in Enzymology; Academic Press: New York, NY, 1966; pp. 565–571.
   Google Scholar
• Sambrook, J.; Fritsch, E. F.; Maniatis, T. Molecular Cloning: A Laboratory Manual. 2nd ed.; Cold Spring Harbor Laboratory Press: New York, NY, 1989.
   Google Scholar
• Frank, J. A.; Reich, C. I.; Sharma, S.; Weisbaum, J. S.; Wilson, B. A.; Olsen, G. J. Critical Evaluation of Two Primers Commonly Used for Amplification of Bacterial 16S rRNA Genes. Appl. Environ. Microbiol. 2008, 74, 2461–2470.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding. Anal. Biochem. 1976, 72, 248–254.
   PubMed Web of Science ®Google Scholar
• Saishin, N.; Ueta, M.; Wada, A; Yamamoto, I. Purification and Characterization of α-Galactosidase I from Bifidobacterium longum subsp. longum JCM 7052. J. Biol. Micromol. 2010, 10, 13–22. 
   Google Scholar
• Layne, E. Spectrophotometric and Turbidimetric Methods for Measuring Proteins. Method Enzymol. 1957, 3, 447–454.
   Web of Science ®Google Scholar
• Blum, H.; Beier, H.; Gross, H. J. Improved Silver Staining of Plant Proteins, RNA and DNA in Polyacrylamide Gels. Electrophoresis. 1987, 8, 93–99. DOI: 10.1002/elps.1150080203.
   Web of Science ®Google Scholar
• Laemmli, U. K.; Favre, M. Cleavage of Structural Proteins during the Assembly of the Head of Bacteriophage T4. Nature 1970, 227, 680–682. DOI: 10.1038/227680a0.
   PubMed Web of Science ®Google Scholar
• Wong, H. C.; Hu, C. A.; Yeh, H. L.; Su, W.; Lu, H. C.; Lin, C. F. Production, Purification, and Characterization of α-Galactosidase from Monascus pilosus. Appl. Microbiol. Biotechnol. 1986, 52, 1147–1152.
   Google Scholar
• Huang, Y.; Zhang, H.; Ben, P.; Duan, Y.; Lu, M.; Li, Z.; Cui, Z. Characterization of a Novel GH36 α-Galactosidase from Bacillus megaterium and Its Application in Degradation of Raffinose Family Oligosaccharides. Int. J. Biol. Macromol. 2018, 108, 98–104.
   PubMedGoogle Scholar
• Mulimani, V. H. Enzymic Hydrolysis of Raffinose and Stachyose in Soymilk by Alpha-Galactosidase from Gibberella fujikuroi. Biochem. Mol. Biol. Int. 1995, 36, 897–905.
   PubMedGoogle Scholar
• Kotiguda, G.; Kapnoor, S. S.; Kulkarni, D.; Mulimani, V. H. Degradation of Raffinose Oligosaccharides in Soymilk by Immobilized α-Galactosidase of Aspergillus oryzae. J. Microbiol. Biotechnol. 2007, 17, 1430–1436.
   PubMedGoogle Scholar
• Fialho, LdS.; Guimarães, V. M.; Callegari, C. M.; Reis, A. P.; Barbosa, D. S.; Borges, E. E. L.; Moreira, M. A.; de Rezende, S. T. Characterization and Biotechnological Application of an Acid α-Galactosidase from Tachigali multijuga Benth. seeds. Phytochemistry 2008, 69, 2579–2585.
   PubMedGoogle Scholar
• Jadaun, J. S.; Narnoliya, L. K.; Agarwal, N.; Singh, S. P. Catalytic Biosynthesis of Levan and Short-Chain Fructooligosaccharides from Sucrose-Containing Feedstocks by Employing the Levansucrase from Leuconostoc mesenteroides MTCC10508. Int. J. Biol. Macromol. 2019, 127, 486–495.
   PubMedGoogle Scholar
• Summer, J. B.; Somers, G. F. Dinitrosalicylic Acid for Glucose. In Laboratory Experiments in Biological Chemistry; Academic Press: New York, NY, 1954; pp. 34–39.
   Google Scholar
• Rodino, S. B.; Butu, M.; Negoescu, C.; Caunii, A.; Cristina, R. T.; Butnariu, M. Spectrophotometric Method for Quantitative Determination of Nystatin Antifungal Agent in Pharmaceutical Formulations. Dig. J. Nanomater. Biostruct. 2014, 9, 1215–1222.
   Web of Science ®Google Scholar
• Patil, A. G.; Praveen Kumar, S. K.; Mulimani, V. H.; Veeranagouda, Y.; Lee, K. α-Galactosidase from Bacillus megaterium VHM1 and Its Application in Removal of Flatulence-Causing Factors from Soymilk. J. Microbiol. Biotechnol. 2010, 20, 1546–1554.
   PubMed Web of Science ®Google Scholar
• Gherardini, F.; Babcock, M. A.; Salyers, A. A. Purification and Characterization of Two Alpha-Galactosidases Associated with Catabolism of Guar Gum and Other Alpha-Galactosides by Bacteroides ovatus. J. Bacteriol. 1985, 161, 500–506.
   PubMedGoogle Scholar
• Holt, S. M.; Teresi, J. M.; Cote, G. L. Influence of Alternansucrase‐Derived Oligosaccharides and Other Carbohydrates on α‐Galactosidase and α‐Glucosidase Activity in Bifidobacterium adolescentis. Lett. Appl. Microbiol. 2008, 46, 73–79.
   PubMed Web of Science ®Google Scholar
• Garro, M. S.; de Valdez, G. F.; Oliver, G.; de Giori, G. S. Purification of α-Galactosidase from Lactobacillus fermentum. J. Biotechnol. 1996, 45, 103–109. DOI: 10.1016/0168-1656(95)00149-2.
   Google Scholar
• Gote, M.; Umalkar, H.; Khan, I.; Khire, J. Thermostable α-Galactosidase from Bacillus stearothermophilus (NCIM 5146) and Its Application in the Removal of Flatulence Causing Factors from Soymilk. Process Biochem. 2004, 39, 1723–1729. DOI: 10.1016/j.procbio.2003.07.008.
   Web of Science ®Google Scholar
• Lee, J.; Park, I.; Cho, J. Production and Partial Characterization of α-Galactosidase Activity from an Antarctic Bacterial Isolate, Bacillus sp. LX-1. Afr. J. Biotechnol. 2012, 11, 12396–12405.
   Google Scholar
• Li, X.; Yang, L.; Yan, P.; Zuo, F.; Jin, F. Factors Regulating Production of α‐Galactosidase from Bacillus sp. JF2. Lett. Appl. Microbiol. 1997, 25, 1–4. DOI: 10.1046/j.1472-765x.1997.00155.x.
   PubMedGoogle Scholar
• Sanjay, C.; Sushma, S. Isolation, Identification and Media Optimization of Thermostable Alpha Galactosidase Producing Geobacillus sp. Res. J. Chem. Environ. 2010, 14, 22–26.
   Google Scholar
• Kandari, S.; Choi, Y. J.; Lee, B. H. Purification and Characterization of Hydrolytic and Transgalactosyl α-Galactosidase from Lactobacillus helveticus ATCC 10797. Eur. Food Res. Technol. 2014, 239, 877–884. DOI: 10.1007/s00217-014-2284-y.
   Google Scholar
• Delente, J.; Johnson, J. H.; Kuo, M. J.; O'Connor, R. J.; Weeks, L. E. Production of a New Thermostable Neutral α‐Galactosidase from a Strain of Bacillus stearothermophilus. Biotechnol. Bioeng. 1974, 16, 1227–1243.
   PubMed Web of Science ®Google Scholar
• Brouns, S. J. J.; Smits, N.; Wu, H.; Snijders, A. P. L.; Wright, P. C.; de Vos, W. M.; van der Oost, J. Identification of a Novel α-Galactosidase from the Hyperthermophilic Archaeon Sulfolobus solfataricus. J. Bacteriol. 2006, 188, 2392–2399.
   PubMed Web of Science ®Google Scholar
• Lokuge, M. A.; Mathew, C. D. Isolation from Soil of Bacteria Producing Extracellular Alpha Galactosidase. J. Natl. Sci. Found. Sri. 2000, 9, 28.
   Google Scholar
• LeBlanc, J. G.; Garro, M. S.; de Giori, G. S. Effect of pH on Lactobacillus fermentum Growth, Raffinose Removal, α-Galactosidase Activity and Fermentation Products. Appl. Microbiol. Biotechnol. 2004, 65, 119–123.
   PubMedGoogle Scholar
• Ganter, C.; Böck, A.; Buckel, P.; Mattes, R. Production of Thermostable, Recombinant α-Galactosidase Suitable for Raffinose Elimination from Sugar Beet Syrup. J. Biotechnol. 1988, 8, 301–310. DOI: 10.1016/0168-1656(88)90022-3.
   Google Scholar
• Anisha, G. S.; John, R. P.; Prema, P. Biochemical and Hydrolytic Properties of Multiple Thermostable α-Galactosidases from Streptomyces griseoloalbus: Obvious Existence of a Novel Galactose-Tolerant Enzyme. Process Biochem. 2009, 44, 327–333. DOI: 10.1016/j.procbio.2008.11.009.
   Web of Science ®Google Scholar
• Duffaud, G. D.; McCutchen, C. M.; Leduc, P.; Parker, K. N.; Kelly, R. M. Purification and Characterization of Extremely Thermostable Beta-Mannanase, Beta-Mannosidase, and Alpha-Galactosidase from the Hyperthermophilic Eubacterium Thermotoga neapolitana 5068. Appl. Environ. Microbiol. 1997, 63, 169–177.
   PubMed Web of Science ®Google Scholar
• Tzortzis, G.; Jay, A. J.; Baillon, M. L.; Gibson, G. R.; Rastall, R. A. Synthesis of α-Galactooligosaccharides with α-Galactosidase from Lactobacillus reuteri of Canine Origin. Appl. Microbiol. Biotechnol. 2003, 63, 286–292. DOI: 10.1007/s00253-003-1426-0.
   PubMed Web of Science ®Google Scholar
• Talbot, G.; Sygusch, J. Purification and Characterization of Thermostable Beta-Mannanase and Alpha-Galactosidase from Bacillus stearothermophilus. Appl. Environ. Microbiol. 1990, 56, 3505–3510.
   PubMed Web of Science ®Google Scholar
• Carrera-Silva, E. A.; Silvestroni, A.; LeBlanc, J. G.; Piard, J. C.; de Giori, G. S.; Sesma, F. A Thermostable α-Galactosidase from Lactobacillus fermentum CRL722: Genetic Characterization and Main Properties. Curr. Microbiol. 2006, 53, 374–378.
   PubMed Web of Science ®Google Scholar
• Fridjonsson, O.; Watzlawick, H.; Gehweiler, A.; Rohrhirsch, T.; Mattes, R. Cloning of the Gene Encoding a Novel Thermostable α-Galactosidase from Thermus brockianus ITI360. Appl. Environ. Microbiol. 1999, 65, 3955–3963.
   PubMed Web of Science ®Google Scholar
• Chaudet, M. M.; Allen, J. L.; Rose, D. R. Expression and Purification of Two Family GH31 α-Glucosidases from Bacteroides thetaiotaomicron. Protein Expr. Purif. 2012, 86, 135–141.
   PubMedGoogle Scholar
• King, M. R.; Yernool, D. A.; Eveleigh, D. E.; Chassy, B. M. Thermostable α-Galactosidase from Thermotoga neapolitana: Cloning, Sequencing and Expression. FEMS Microbiol. Lett. 1998, 163, 37–42.
   PubMed Web of Science ®Google Scholar
• Kondoh, K.; Morisaki, K.; Kim, W. D.; Park, G. G.; Kaneko, S.; Kobayashi, H. Cloning and Expression of the Gene Encoding Streptomyces coelicolor A3 (2) α-Galactosidase Belonging to Family 36. Biotechnol. Lett. 2005, 27, 641–647.
   PubMed Web of Science ®Google Scholar
• Siddiqi, M. Z.; Srinivasan, S.; Park, H. Y.; Im, W. T. Exploration and Characterization of Novel Glycoside Hydrolases from the Whole Genome of Lactobacillus ginsenosidimutans and Enriched Production of Minor Ginsenoside Rg3 (S) by a Recombinant Enzymatic Process. Biomolecules 2020, 10, 288. DOI: 10.3390/biom10020288.
   PubMedGoogle Scholar
• Shin, Y.-J.; Woo, S.-H.; Jeong, H.-M.; Kim, J.-S.; Ko, D.-S.; Jeong, D.-W.; Lee, J.-H.; Shim, J.-H. Characterization of Novel α-Galactosidase in Glycohydrolase Family 97 from Bacteroides thetaiotaomicron and Its Immobilization for Industrial Application. Int. J. Biol. Macromol. 2020, 152, 727–734.
   PubMedGoogle Scholar
• Yoon, M. Y.; Hwang, H. J. Reduction of Soybean Oligosaccharides and Properties of α-d-Galactosidase from Lactobacillus curvatus R08 and Leuconostoc mesenteriodes JK55. Food Microbiol. 2008, 25, 815–823. DOI: 10.1016/j.fm.2008.04.008.
   PubMed Web of Science ®Google Scholar
• Page, M. J.; Di Cera, E. Role of Na+ and K+ in Enzyme Function. Physiol. Rev. 2006, 86, 1049–1092. DOI: 10.1152/physrev.00008.2006.
   PubMed Web of Science ®Google Scholar
• Heyda, J.; Pokorná, J.; Vrbka, L.; Vácha, R.; Jagoda-Cwiklik, B.; Konvalinka, J.; Jungwirth, P.; Vondrášek, J. Ion Specific Effects of Sodium and Potassium on the Catalytic Activity of HIV-1 Protease. Phys. Chem. Chem. Phys. 2009, 11, 7599–7604. DOI: 10.1039/b905462f.
   PubMed Web of Science ®Google Scholar
• Guo, Y.; Song, Y.; Qiu, Y.; Shao, X.; Wang, H.; Song, Y. Purification of Thermostable α‐Galactosidase from Irpex lacteus and Its Use for Hydrolysis of Oligosaccharides. J. Basic Microbiol. 2016, 56, 448–458. DOI: 10.1002/jobm.201500668.
   PubMedGoogle Scholar
• Hu, Y.; Tian, G.; Zhao, L.; Wang, H.; Ng, T. B. A Protease-Resistant α-Galactosidase from Pleurotus djamor with Broad pH Stability and Good Hydrolytic Activity toward Raffinose Family Oligosaccharides. Int. J. Biol. Macromol. 2017, 94, 122–130. DOI: 10.1016/j.ijbiomac.2016.10.005.
   PubMedGoogle Scholar
• Ramadevi, M.; Deepesh, P.; Juby Elsa, J.; Gaurav Singh, K. Low Molecular Weight α-Galactosidase from Black Gram (Vigna mungo): Purification, Characterization, and Insights towards Thermal Denaturation. Int. J. Biol. Macromol. 2018, 119, 770–778.
   PubMedGoogle Scholar
• Park, I.; Lee, J.; Cho, J. Partial Characterization of α-Galactosidic Activity from the Antarctic Bacterial Isolate, Paenibacillus sp. LX-20 as a Potential Feed Enzyme Source. Asian Australas. J. Anim. Sci. 2012, 25, 852–860. DOI: 10.5713/ajas.2011.11501.
   PubMedGoogle Scholar
• Sirisha, E.; Potumarthi, R.; Naveen, A.; Mangamoori, L. N. Purification and Characterisation of Intracellular Alpha-Galactosidases from Acinetobacter sp. 3 Biotech. 2015, 5, 925–932.
   PubMedGoogle Scholar
• King, M. R.; White, B. A.; Blaschek, H. P.; Chassy, B. M.; Mackie, R. I.; Cann, I. K. Purification and Characterization of a Thermostable α-Galactosidase from Thermoanaerobacterium polysaccharolyticum. J. Agric. Food Chem. 2002, 50, 5676–5682.
   PubMedGoogle Scholar
• Farzadi, M.; Khatami, S.; Mousavi, M.; Amirmozafari, N. Purification and Characterization of α-Galactosidase from Lactobacillus acidofillus. Afr. J. Biotechnol. 2011, 10, 1873–1879.
   Google Scholar
• Gong, W.; Xu, L.; Gu, G.; Lu, L.; Xiao, M. Efficient and Regioselective Synthesis of Globotriose by a Novel α-Galactosidase from Bacteroides fragilis. Appl. Microbiol. Biotechnol. 2016, 100, 6693–6702.
   PubMedGoogle Scholar
• Delgado-Fernandez, P.; Plaza-Vinuesa, L.; Hernandez-Hernandez, O.; de Las Rivas, B.; Corzo, N.; Muñoz, R.; Moreno, F. J. Unravelling the Carbohydrate Specificity of MelA from Lactobacillus plantarum WCFS1: An α-Galactosidase Displaying Regioselective Transgalactosylation. Int. J. Biol. Macromol. 2020, 153, 1070–1079.
   PubMedGoogle Scholar
• Panwar, D.; Shubhashini, A.; Chaudhari, S. R.; Prashanth, K. H.; Kapoor, M. GH36 α-Galactosidase from Lactobacillus plantarum WCFS1 Synthesize Gal-α-1,6 Linked Prebiotic α-Galactooligosaccharide by Transglycosylation. Int. J. Biol. Macromol. 2020, 144, 334–342.
   PubMedGoogle Scholar
• Van Laere, K. M. J.; Hartemink, R.; Beldman, G.; Pitson, S.; Dijkema, C.; Schols, H. A.; Voragen, A. G. J. Transglycosidase Activity of Bifidobacterium adolescentis DSM 20083 α-Galactosidase. Appl. Microbiol. Biotechnol. 1999, 52, 681–688. DOI: 10.1007/s002530051579.
   PubMed Web of Science ®Google Scholar
• Wang, J.; Yang, X.; Yang, Y.; Liu, Y.; Piao, X.; Cao, Y. Characterization of a Protease-Resistant α-Galactosidase from Aspergillus oryzae YZ1 and Its Application in Hydrolysis of Raffinose Family Oligosaccharides from Soymilk. Int. J. Biol. Macromol. 2020, 158, 708–720.
   PubMedGoogle Scholar
• Butu, M.; Butnariu, M.; Rodino, S.; Butu, A. Study of Zingiberene from Lycopersicon esculentum Fruit by Mass Spectrometry. Dig. J. Nanomater. Biostruct. 2014, 9, 935–941.
   Web of Science ®Google Scholar
• Oh, S. Y.; Youn, S. Y.; Park, M. S.; Baek, N. I.; Ji, G. E. Synthesis of Stachyobifiose Using Bifidobacterial α-Galactosidase Purified from Recombinant Escherichia coli. J. Agric. Food Chem. 2018, 66, 1184–1190. DOI: 10.1021/acs.jafc.7b04703.
   PubMedGoogle Scholar
• Xia, X.; Dai, Y.; Wu, H.; Liu, X.; Wang, Y.; Yin, L.; Wang, Z.; Li, X.; Zhou, J. Kombucha Fermentation Enhances the Health-Promoting Properties of Soymilk Beverage. J. Funct. Foods 2019, 62, 103549. DOI: 10.1016/j.jff.2019.103549.
   Web of Science ®Google Scholar
• Jindou, S.; Karita, S.; Fujino, E.; Fujino, T.; Hayashi, H.; Kimura, T.; Sakka, K.; Ohmiya, K. α-Galactosidase Aga27A, an Enzymatic Component of the Clostridium josui Cellulosome. J. Bacteriol. 2002, 184, 600–604.
   PubMed Web of Science ®Google Scholar
• Schröder, C.; Janzer, V. A.; Schirrmacher, G.; Claren, J.; Antranikian, G. Characterization of Two Novel Heat-Active α-Galactosidases from Thermophilic Bacteria. Extremophiles 2017, 21, 85–94.
   PubMedGoogle Scholar