Abstract
α-Galactosidase (α-D-galactosidase galactohydrolase; EC 3.2.1.22), is an industrially important enzyme that hydrolyzes the galactose residues in galactooligosaccharides and polysaccharides. The industrial production of α-galactosidase is currently insufficient owing to the high production cost, low production efficiency and low enzyme activity. Recent years have witnessed an increase in the worldwide research on molecular techniques to improve the production efficiency of microbial α-galactosidases. Cloning and overexpression of the gene sequences coding for α-galactosidases can not only increase the enzyme yield but can confer industrially beneficial characteristics to the enzyme protein. This review focuses on the molecular advances in the overexpression of α-galactosidases in bacterial and yeast/fungal expression systems. Recombinant α-galactosidases have improved biochemical and hydrolytic properties compared to their native counterparts. Metabolic engineering of microorganisms to produce high yields of α-galactosidase can also assist in the production of value-added products. Developing new variants of α-galactosidases through directed evolution can yield enzymes with increased catalytic activity and altered regioselectivity. The bottlenecks in the recombinant production of α-galactosidases are also discussed. The knowledge about the hurdles in the overexpression of recombinant proteins illuminates the emerging possibilities of developing a successful microbial cell factory and widens the opportunities for the production of industrially beneficial α-galactosidases.
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Abbreviations
- RFO:
-
Raffinose family oligosaccharides
- CAZy:
-
Carbohydrate active enzymes
- GH:
-
Glycoside hydrolase
- PUL:
-
Polysaccharide utilization locus
- ATP:
-
Adenosine triphosphate
- AOX:
-
Alcohol oxidase
- gpd:
-
Glyceraldehyde-3-phosphate dehydrogenase
- epPCR:
-
Error-prone polymerase chain reaction
- FRISM:
-
Focused rational iterative site-specific mutagenesis
References
Álvarez-Cao ME, Rico-Díaz A, Cerdán ME, Becerra M, González-Siso MI (2018) Valuation of agro-industrial wastes as substrates for heterologous production of α-galactosidase. Microb Cell Fact 17:137. https://doi.org/10.1186/s12934-018-0988-6
Álvarez-Cao ME, Cerdán ME, González-Siso MI, Becerra M (2019a) Optimization of Saccharomyces cerevisiae α-galactosidase production and application in the degradation of raffinose family oligosaccharides. Microb Cell Fact 18:1–17. https://doi.org/10.1186/s12934-019-1222-x
Álvarez-Cao ME, Cerdán ME, González-Siso MI, Becerra M (2019b) Bioconversion of beet molasses to alpha-galactosidase and ethanol. Front Microbiol 10:405. https://doi.org/10.3389/fmicb.2019.00405
An JL, Zhang WX, Wu WP, Chen GJ, Liu WF (2019) Characterization of a highly stable α-galactosidase from thermophilic Rasamsonia emersonii heterologously expressed in a modified Pichia pastoris expression system. Microb Cell Fact 18:180. https://doi.org/10.1186/s12934-019-1234-6
Anisha GS (2022a) Microbial α-galactosidases: efficient biocatalysts for bioprocess technology. Bioresour Technol 344:126293. https://doi.org/10.1016/j.biortech.2021.126293
Anisha GS (2022b) Biopharmaceutical applications of α-galactosidases. Biotechnol Appl Biochem. https://doi.org/10.1002/bab.2349
Aulitto M, Fusco S, Fiorentino G, Limauro D, Pedone E, Bartolucci S, Contursi P (2017) Thermus thermophilus as source of thermozymes for biotechnological applications: homologous expression and biochemical characterization of an α-galactosidase. Microb Cell Fact 16:28. https://doi.org/10.1186/s12934-017-0638-4
Aulitto M, Fusco FA, Fiorentino G, Bartolucci S, Contursi P, Limauro D (2018) A thermophilic enzymatic cocktail for galactomannans degradation. Enzyme Microb Technol 111:7–11. https://doi.org/10.1016/J.ENZMICTEC.2017.12.008
Baghban R, Farajnia S, Rajabibazl M, Ghasemi Y, Mafi A, Hoseinpoor R, Rahbarnia L, Aria M (2019) Yeast expression systems: overview and recent advances. Mol Biotechnol 61:365–384. https://doi.org/10.1007/s12033-019-00164-8
Bakunina I, Slepchenko L, Anastyuk S, Isakov V, Likhatskaya G, Kim N, Tekutyeva L, Son O, Balabanova L (2018) Characterization of properties and transglycosylation abilities of recombinant α-galactosidase from cold-adapted marine bacterium Pseudoalteromonas KMM 701 and its C494N and D451A mutants. Mar Drugs 16:349. https://doi.org/10.3390/md16100349
Berka RM, Grigoriev IV, Otillar R, Salamov A, Grimwood J, Reid I, Ishmael N, John T, Darmond C, Moisan MC, Henrissat B, Coutinho PM, Lombard V, Natvig DO, Lindquist E, Schmutz J, Lucas S, Harris P, Powlowski J, Bellemare A, Taylor D, Butler G, de Vries RP, Allijn IE, van den Brink J, Ushinsky S, Storms R, Powell AJ, Paulsen IT, Elbourne LDH, Baker SE, Magnuson J, LaBoissiere S, Clutterbuck AJ, Martinez D, Wogulis M, de Leon AL, Rey MW, Tsang A (2011) Comparative genomic analysis of the thermophilic biomass-degrading fungi Myceliophthora thermophila and Thielavia terrestris. Nat Biotechnol 29:922–927. https://doi.org/10.1038/nbt.1976
Bhatia S, Singh A, Batra N, Singh J (2020) Microbial production and biotechnological applications of α-galactosidase. Int J Biol Macromol 150:1294–1313. https://doi.org/10.1016/j.ijbiomac.2019.10.140
Bobrov KS, Borisova AS, Eneyskaya EV, Ivanen DR, Shabalin KA, Kulminskaya AA, Rychkov GN (2013) Improvement of the efficiency of transglycosylation catalyzed by α-galactosidase from Thermotoga maritima by protein engineering. Biochem 78:1112–1123. https://doi.org/10.1134/S0006297913100052
Brouns SJJ, Smits N, Wu H, Snijders APL, Wright PC, De Vos WM, van der Oost J (2006) Identification of a novel α-galactosidase from the hyperthermophilic archaeon Sulfolobus solfataricus. J Bacteriol 188:2392–2399. https://doi.org/10.1128/JB.188.7.2392
Bruel L, Sulzenbacher G, Tison MC, Pujol A, Nicoletti C, Perrier J, Galinier A, Ropartz D, Fons M, Pompeo F, Giardina T (2011) α-galactosidase/sucrose kinase (AgaSK), a novel bifunctional enzyme from the human microbiome coupling galactosidase and kinase activities. J Biol Chem 286:40814–40823. https://doi.org/10.1074/jbc.M111.286039
Çalcı E, Önal S (2022) Comparative affinity immobilization of α-galactosidase on chitosan functionalized with concanavalin A and its useability for the hydrolysis of raffinose. React Funct Polym. https://doi.org/10.1016/j.reactfunctpolym.2022.105181
Çelem EB, Önal S (2022) Sepabeads EC-EP immobilized α-galactosidase: Immobilization, characterization and application in the degradation of raffinose-type oligosaccharides. Process Biochem 116:136–147. https://doi.org/10.1016/j.procbio.2022.02.020
Cereghino JL, Cregg JM (2000) Heterologous protein expression in the methylotrophic yeast Pichia pastoris. FEMS Microbiol Rev 24:45–66. https://doi.org/10.1111/j.1574-6976.2000.tb00532.x
Chen Y, Zhang B, Pei H, Lv J, Yang W, Cao Y, Dong B (2012) Directed evolution of Penicillium janczewskii zalesk α-galactosidase toward enhanced activity and expression in Pichia pastoris. Appl Biochem Biotechnol 168:638–650. https://doi.org/10.1007/s12010-012-9806-5
Chen Z, Yan Q, Jiang Z, Liu Y, Li Y (2015) High-level expression of a novel α-galactosidase gene from Rhizomucor miehei in Pichia pastoris and characterization of the recombinant enyzme. Protein Expr Purif 110:107–114. https://doi.org/10.1016/J.PEP.2015.02.015
Chen YP, Liaw LL, Kuo JT, Wu HT, Wang GH, Chen XQ, Tsai CF, Young CC (2019) Evaluation of synthetic gene encoding α-galactosidase through metagenomic sequencing of paddy soil. J Biosci Bioeng 128:274–282. https://doi.org/10.1016/J.JBIOSC.2019.03.006
Chen X, Wang X, Liu Y, Zhang R, Zhang L, Zhan R, Wang S, Wang K (2021) Biochemical analyses of a novel thermostable GH5 endo β-1,4-mannanase with minor β-1,4-glucosidic cleavage activity from Bacillus sp. KW1 and its synergism with a commercial α-galactosidase on galactomannan hydrolysis. Int J Biol Macromol 166:778–788. https://doi.org/10.1016/J.IJBIOMAC.2020.10.235
Cobb RE, Chao R, Zhao H (2013) Directed evolution: past, present and future. AIChE J 59:1432–1440. https://doi.org/10.1002/aic.13995
Currin A, Parker S, Robinson CJ, Takano E, Scrutton NS, Breitling R (2021) The evolving art of creating genetic diversity: from directed evolution to synthetic biology. Biotechnol Adv 50:107762. https://doi.org/10.1016/j.biotechadv.2021.107762
Daly P, Van Munster JM, Blythe MJ, Ibbett R, Kokolski M, Gaddipati S, Lindquist E, Singan VR, Barry KW, Lipzen A, Ngan CY, Petzold CJ, Chan LJG, Pullan ST, Delmas S, Waldron PR, Grigoriev IV, Tucker GA, Simmons BA, Archer DB (2017) Expression of Aspergillus niger CAZymes is determined by compositional changes in wheat straw generated by hydrothermal or ionic liquid pretreatments. Biotechnol Biofuels 10:1–19. https://doi.org/10.1186/s13068-017-0700-9
de Vries RP, Riley R, Wiebenga A, Aguilar-osorio G, Amillis S, Uchima CA, Anderluh G, Asadollahi M, Askin M, Barry K, Battaglia E, Bayram Ö, Benocci T, Braus-stromeyer SA, Caldana C, Cánovas D, Ricardo A, Damásio DL, Diallinas G, Emri T, Fekete E, Flipphi M (2017) Comparative genomics reveals high biological diversity and specific adaptations in the industrially and medically important fungal genus Aspergillus. Genome Biol 18:1–45. https://doi.org/10.1186/s13059-017-1151-0
Dilokpimol A, Peng M, Di Falco M, Chin A, Woeng T, Hegi RMW, Granchi Z, Tsang A, Hildén KS, Mäkelä MR, de Vries RP (2020) Penicillium subrubescens adapts its enzyme production to the composition of plant biomass. Bioresour Technol 311:123477. https://doi.org/10.1016/j.biortech.2020.123477
Dion M, Nisole A, Spangenberg P, Andre C, Glottin-Fleury A, Mattes R, Tellier C, Rabiller C (2001) Modulation of the regioselectivity of a Bacillus α-galactosidase by directed evolution. Glycoconj J 18:215–223. https://doi.org/10.1023/a:1012448522187
Fei Y, Jiao WJ, Wang Y, Liang J, Liu G, Li L (2020) Cloning and expression of a novel α-galactosidase from Lactobacillus amylolyticus L6 with hydrolytic and transgalactosyl properties. PLoS ONE 15:1–12. https://doi.org/10.1371/journal.pone.0235687
Fernández FJ, López-Estepa M, Querol-García J, Vega MC (2016) Production of protein complexes in non-methylotrophic and methylotrophic yeasts. Adv Exp Med Biol 896:137–153. https://doi.org/10.1007/978-3-319-27216-0_9
Fridjonsson O, Watzlawick H, Gehweiler A, Rohrhirsch T, Mattes R (1999) Cloning of the gene encoding a novel thermostable α-galactosidase from Thermus brockianus ITI360. Appl Environ Microbiol 65:3955–3963. https://doi.org/10.1128/aem.65.9.3955-3963.1999
Fujino Y, Goda S, Suematsu Y, Doi K (2020) Development of a new gene expression vector for Thermus thermophilus using a silica—inducible promoter. Microb Cell Fact 19:1–12. https://doi.org/10.1186/s12934-020-01385-2
Guerfal M, Ryckaert S, Jacobs PP, Ameloot P, Van Craenenbroeck K, Derycke R, Callewaert N (2010) The HAC1 gene from Pichia pastoris: characterization and effect of its overexpression on the production of secreted, surface displayed and membrane proteins. Microb Cell Fact 9:1–12. https://doi.org/10.1186/1475-2859-9-49
Gürkök S, Söyler B, Biely P, Ögel ZB (2010) Cloning and heterologous expression of the extracellular alpha-galactosidase from Aspergillus fumigatus in Aspergillus sojae under the control of gpdA promoter. J Mol Catal B 64:146–149. https://doi.org/10.1016/J.MOLCATB.2009.09.012
Gurkok S, Cekmecelioglu D, Ogel ZB (2011) Optimization of culture conditions for Aspergillus sojae expressing an Aspergillus fumigatus α-galactosidase. Bioresour Technol 102:4925–4929. https://doi.org/10.1016/j.biortech.2011.01.036
Hidalgo A, Betancor L, Moreno R, Zafra O, Cava F (2004) Thermus thermophilus as a cell factory for the production of a thermophilic Mn-dependent catalase which fails to be synthesized in an active form in Escherichia coli. Appl Environ Microbiol 70:3839–3844. https://doi.org/10.1128/AEM.70.7.3839
Hinz S, Doeswijk C, Schipperus R, Broek L, Vincken JP, Voragen A (2006) Increasing the transglycosylation activity of α-galactosidase from Bifidobacterium adolescentis DSM 20083 by site-directed mutagenesis. Biotechnol Bioeng 93:122–131. https://doi.org/10.1002/bit.20713
Hsieh PC, Vaisvila R (2013) Protein engineering: single or multiple site-directed mutagenesis. Methods Mol Biol 978:173–186. https://doi.org/10.1007/978-1-62703-293-3_13
Jang JM, Yang Y, Wang R, Bao H, Yuan H, Yang J (2019) Characterization of a high performance α-galactosidase from Irpex lacteus and its usage in removal of raffinose family oligosaccharides from soymilk. Int J Biol Macromol 131:1138–1146. https://doi.org/10.1016/J.IJBIOMAC.2019.04.060
Jourdier E, Baudry L, Parodi DP, Vicq Y, Koszul R, Margeot A, Marbouty M, Bidard F (2017) Proximity ligation scaffolding and comparison of two Trichoderma reesei strains genomes. Biotechnol Biofuels 10:1–13. https://doi.org/10.1186/s13068-017-0837-6
Juturu V, Wu JC (2018) Heterologous protein expression in Pichia pastoris: latest research progress and applications. ChemBioChem 19:7–21. https://doi.org/10.1002/cbic.201700460
Karbalaei M (2020) Pichia pastoris : A highly successful expression system for optimal synthesis of heterologous proteins. J Cell Physiol. https://doi.org/10.1002/jcp.29583
Katrolia P, Jia H, Yan Q, Song S, Jiang Z, Xu H (2012) Characterization of a protease-resistant α-galactosidase from the thermophilic fungus Rhizomucor miehei and its application in removal of raffinose family oligosaccharides. Bioresour Technol 110:578–586. https://doi.org/10.1016/J.BIORTECH.2012.01.144
Kikuchi A, Okuyama M, Kato K, Osaki S, Ma M, Kumagai Y, Matsunaga K, Klahan P, Tagami T, Yao M, Kimura A (2017) A novel glycoside hydrolase family 97 enzyme: bifunctional β-L-arabinopyranosidase/α-galactosidase from Bacteroides thetaiotaomicron. Biochimie 142:41–50. https://doi.org/10.1016/j.biochi.2017.08.003
Kirubakaran R, Aruljothi KN, Revathi S, Shameem N, Parray JA (2020) Emerging priorities for microbial metagenome research. Bioresour Technol Rep 11:100485. https://doi.org/10.1016/j.biteb.2020.100485
Lafond M, Tauzin AS, Bruel L, Laville E, Lombard V, Esque J, André I, Vidal N, Pompeo F, Quinson N, Perrier J, Fons M, Potocki-Veronese G, Giardina T (2020) α-Galactosidase and sucrose-kinase relationships in a bi-functional AgaSK enzyme produced by the human gut symbiont Ruminococcus gnavus E1. Front Microbiol 11:1–16. https://doi.org/10.3389/fmicb.2020.579521
Lee A, Choi KH, Yoon D, Kim S, Cha J (2017) Characterization of a thermostable glycoside hydrolase family 36 α-galactosidase from Caldicellulosiruptor bescii. J Biosci Bioeng 124:289–295. https://doi.org/10.1016/J.JBIOSC.2017.04.011
Lee MC, Kim SY, Song J, Lee YS, Sim JS, Hahn BS (2018) Isolation and characterization of a halotolerant and protease-resistant α-galactosidase from the gut metagenome of Hermetia illucens. J Biotechnol 279:47–54. https://doi.org/10.1016/j.biotec.2018.05.003
Lenders M, Brand E (2021) Fabry disease : the current treatment landscape. Drugs 81:635–645. https://doi.org/10.1007/s40265-021-01486-1
Linares CN, Dilokpimol A, Stålbrand H, Mäkelä MR, de Vries RP (2020) 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. Bioresour Technol 295:122258. https://doi.org/10.1016/j.biortech.2019.122258
Liu Y, Yang S, Yan Q, Liu J, Jiang Z (2018) High-level expression of a novel protease-resistant α-galactosidase from Thielavia terrestris. Process Biochem 71:82–91. https://doi.org/10.1016/J.PROCBIO.2018.05.025
Liu Y, Yan Q, Guan L, Jiang Z, Yang S (2020) Biochemical characterization of a novel protease-resistant α-galactosidase from Paecilomyces thermophila suitable for raffinose family oligosaccharides degradation. Process Biochem 94:370–379. https://doi.org/10.1016/j.procbio.2020.04.013
Mahalapbutr P, Klaewkla M, Charoenwongpaiboon T (2022) Unraveling the effect of A143T, P205T and D244N mutations in α-galactosidase A on its catalytic activity and susceptibility to globotriaosylceramide and iminosugar 1-deoxygalactonojirimycin chaperone. J Mol Liq 353:118790. https://doi.org/10.1016/j.molliq.2022.118790
Manas NHA, Md Illias R, Mahadi NM (2018) Strategy in manipulating transglycosylation activity of glycosyl hydrolase for oligosaccharide production. Crit Rev Biotechnol 38:272–293. https://doi.org/10.1080/07388551.2017.1339664
Martens EC, Lowe EC, Chiang H, Pudlo NA, Wu M, McNulty NP, Abbott DW, Henrissat B, Gilbert HJ, Bolam DN, Gordon JI (2011) Recognition and degradation of plant cell wall polysaccharides by two human gut symbionts. PLoS Biol 9:e1001221. https://doi.org/10.1371/journal.pbio.1001221
Méndez-Líter JA, De Eugenio LI, Nieto-Domínguez M, Prieto A, Martínez J (2021) Hemicellulases from Penicillium and Talaromyces for lignocellulosic biomass valorization: a review. Bioresour Technol 324:124623. https://doi.org/10.1016/j.biortech.2020.124623
Merceron R, Foucault M, Haser R, Mattes R, Watzlawick H, Gouet P (2012) The molecular mechanism of thermostable α-galactosidases AgaA and AgaB explained by X-ray crystallography and mutational studies. J Biol Chem 287:39642–39652. https://doi.org/10.1074/JBC.M112.394114
Mi S, Meng K, Wang Y, Bai Y, Yuan T, Luo H, Yao B (2007) Molecular cloning and characterization of a novel α-galactosidase gene from Penicillium sp. F63 CGMCC 1669 and expression in Pichia pastoris. Enzyme Microb Technol 40:1373–1380. https://doi.org/10.1016/j.enzmictec.2006.10.017
Ndeh D, Rogowski A, Cartmell A, Luis AS, Baslé A, Gray J, Venditto I, Briggs J, Zhang X, Labourel A, Terrapon N, Buffetto F, Nepogodiev S, Xiao Y, Field RA, Zhu Y, O’Neill MA, Urbanowicz BR, York WS, Davies GJ, Abbott DW, Ralet MC, Martens EC, Henrissat B, Gilbert HJ (2017) Complex pectin metabolism by gut bacteria reveals novel catalytic functions. Nature 544:65–70. https://doi.org/10.1038/nature21725
Nevalainen H, Peterson R (2014) Making recombinant proteins in filamentous fungi- are we expecting too much? Front Microbiol 5:1–10. https://doi.org/10.3389/fmicb.2014.00075
Niu C, Wan X (2020) Engineering a trypsin-resistant thermophilic α-galactosidase to enhance pepsin resistance, acidic tolerance, catalytic performance, and potential in the food and feed industry. J Agric Food Chem 68:10560–10573. https://doi.org/10.1021/acs.jafc.0c02175
Panwar D, Shubhashini A, Rama S, Prashanth KVH, Kapoor M (2020) GH36 α-galactosidase from Lactobacillus plantarum WCFS1 synthesize Gal- α -1, 6 linked prebiotic α-galactooligosaccharide by transglycosylation. Int J Biol Macromol 144:334–342. https://doi.org/10.1016/j.ijbiomac.2019.12.032
Peng M, Dilokpimol A, Mäkelä MR, Hildén K, Bervoets S, Riley R, Grigoriev IV, Hainaut M, Henrissat B, De Vries RP, Granchi Z (2017) The draft genome sequence of the ascomycete fungus Penicillium subrubescens reveals a highly enriched content of plant biomass related CAZymes compared to related fungi. J Biotechnol 246:1–3. https://doi.org/10.1016/j.jbiotec.2017.02.012
Qu G, Li A, Acevedo-Rocha CG, Sun Z, Reetz MT (2020) The crucial role of methodology development in directed evolution of selective enzymes. Angew Chem Int Ed 59:13204–13231. https://doi.org/10.1002/anie.201901491
Rahfeld P, Withers SG (2020) Toward universal donor blood: enzymatic conversion of A and B to O type. J Biol Chem 295:325–334. https://doi.org/10.1074/jbc.REV119.008164
Sakamoto T, Tsujitani Y, Fukamachi K, Taniguchi Y, Ihara H (2010) Identification of two GH27 bifunctional proteins with β-L-arabinopyranosidase/α-D-galactopyranosidase activities from Fusarium oxysporum. Appl Microbiol Biotechnol 86:1115–1124. https://doi.org/10.1007/s00253-009-2344-6
Salgado-Bautista D, Volke-Sepúlveda T, Figueroa-Martínez F, Carrasco-Navarro U, Chagolla-Lopez A, Favela-Torres E (2020) Solid-state fermentation increases secretome complexity in Aspergillus brasiliensis. Fungal Biol 124:723–734. https://doi.org/10.1016/j.funbio.2020.04.006
Sawale PD, Shendurse AM, Mohan MS, Patil GR (2017) Isomaltulose (Palatinose)—an emerging carbohydrate. Food Biosci 18:46–52. https://doi.org/10.1016/j.fbio.2017.04.003
Shin YJ, Woo SH, Jeong HM, Kim JS, Ko DS, Jeong DW, Lee JH, Shim JH (2020) Characterization of novel α-galactosidase in glycohydrolase family 97 from Bacteroides thetaiotaomicron and its immobilization for industrial application. Int J Biol Macromol 152:727–734. https://doi.org/10.1016/J.IJBIOMAC.2020.02.232
Silvestroni A, Connes C, Sesma F, De Giori GS, Piard JC (2002) Characterization of the melA locus for α-galactosidase in Lactobacillus plantarum. Appl Environ Microbiol 68:5464–5471. https://doi.org/10.1128/AEM.68.11.5464-5471.2002
Solaiman DKY, Ashby RD, Aneja KK, Crocker NV, Liu Y (2018) Galacto-oligosaccharide hydrolysis by genetically-engineered alpha-galactosidase-producing Pseudomonas chlororaphis strains. Biocatal Agric Biotechnol 13:213–218. https://doi.org/10.1016/j.bcab.2017.12.008
Solaiman DKY, Ashby RD, Crocker NV (2020) Bioprocess for hydrolysis of galacto-oligosaccharides in soy molasses and tofu whey by recombinant Pseudomonas chlororaphis. Biocatal Agric Biotechnol 24:101529. https://doi.org/10.1016/j.bcab.2020.101529
Tauzin AS, Bruel L, Laville E, Nicoletti C, Navarro D, Henrissat B, Perrier J, Potocki-veronese G, Giardina T, Lafond M (2019) Sucrose 6 F-phosphate phosphorylase: a novel insight in the human gut microbiome. Microb Genomics 5:1–16. https://doi.org/10.1099/mgen.0.000253
Vesth TC, Nybo JL, Theobald S, Frisvad JC, Larsen TO, Nielsen KF, Hoof JB, Brandl J, Salamov A, Riley R, Gladden JM, Phatale P, Nielsen MT, Lyhne EK, Kogle ME, Strasser K, Mcdonnell E, Barry K, Clum A, Chen C, Labutti K, Haridas S, Nolan M, Sandor L, Kuo A, Lipzen A, Hainaut M, Drula E, Tsang A, Magnuson JK, Henrissat B, Wiebenga A, Simmons BA, Mäkelä MR, De Vries RP, Grigoriev IV, Mortensen UH, Baker SE, Andersen MR (2018) Investigation of inter- and intraspecies variation through genome sequencing of Aspergillus section Nigri. Nat Genet 50:1688–1695. https://doi.org/10.1038/s41588-018-0246-1
Wakinaka T, Kiyohara M, Kurihara S, Hirata A, Chaiwangsri T, Ohnuma T, Fukamizo T, Katayama T, Ashida H, Yamamoto K (2013) Bifidobacterial α-galactosidase with unique carbohydrate-binding module specifically acts on blood group B antigen. Glycobiology 23:232–240. https://doi.org/10.1093/glycob/cws142
Wang H, Luo H, Li J, Bai Y, Huang H, Shi P, Fan Y, Yao B (2010) An a-galactosidase from an acidophilic Bispora sp. MEY-1 strain acts synergistically with b-mannanase. Bioresour Technol 101:8376–8382. https://doi.org/10.1016/j.biortech.2010.06.045
Wang H, Shi P, Luo H, Huang H, Yang P, Yao B (2014) A thermophilic α-galactosidase from Neosartorya fischeri P1 with high specific activity, broad substrate specificity and significant hydrolysis ability of soymilk. Bioresour Technol 153:361–364. https://doi.org/10.1016/j.biortech.2013.11.078
Wang H, Ma R, Shi P, Huang H (2015) Insights into the substrate specificity and synergy with mannanase of family 27 α-galactosidases from Neosartorya fischeri P1. Appl Microbiol Biotechnol 99:1261–1272. https://doi.org/10.1007/s00253-014-6269-3
Wang C, Wang H, Ma R, Shi P, Niu C, Luo H, Yang P, Yao B (2016) Biochemical characterization of a novel thermophilic α-galactosidase from Talaromyces leycettanus JCM12802 with significant transglycosylation activity. J Biosci Bioeng 121:7–12. https://doi.org/10.1016/j.jbiosc.2015.04.023
Wang ZP, Zhang LL, Liu S, Liu XY, Yu XJ (2019) Whole conversion of soybean molasses into isomaltulose and ethanol by combining enzymatic hydrolysis and successive selective fermentations. Biomolecules 9:1–10. https://doi.org/10.3390/biom9080353
Wang J, Yang X, Yang Y, Liu Y, Piao X, Cao Y (2020a) 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 158:708–720. https://doi.org/10.1016/J.IJBIOMAC.2020.04.256
Wang L, Song L, He X, Teng F, Hu M, Tao Y (2020b) Production of isofloridoside from galactose and glycerol using α-galactosidase from Alicyclobacillus hesperidum. Enzyme Microb Technol 134:109480. https://doi.org/10.1016/j.enzmictec.2019.109480
Wang J, Cao X, Chen W, Xu J, Wu B (2021a) Identification and characterization of a thermostable GH36 α-galactosidase from Anoxybacillus vitaminiphilus WMF1 and Its application in synthesizing isofloridoside by reverse hydrolysis. Int J Mol Sci 22:10778. https://doi.org/10.3390/ijms221910778
Wang Y, Xue P, Cao M, Yu T, Lane ST, Zhao H (2021b) Directed evolution: methodologies and applications. Chem Rev 121:12384–12444. https://doi.org/10.1021/acs.chemrev.1c00260
Xie J, He Z, Wang Z, Wang B, Pan L (2019) Efficient expression of a novel thermophilic fungal β-mannosidase from Lichtheimia ramosa with broad-range pH stability and its synergistic hydrolysis of locust bean gum. J Biosci Bioeng 128:416–423. https://doi.org/10.1016/J.JBIOSC.2019.04.007
Xie J, Wang B, He Z, Pan L (2020) A thermophilic fungal GH36 α-galactosidase from Lichtheimia ramosa and its synergistic hydrolysis of locust bean gum. Carbohydr Res 491:107911. https://doi.org/10.1016/J.CARRES.2020.107911
Xu H, Qin Y, Huang Z, Liu Z (2014) Characterization and site-directed mutagenesis of an α-galactosidase from the deep-sea bacterium Bacillus megaterium. Enzyme Microb Technol 56:46–52. https://doi.org/10.1016/J.ENZMICTEC.2014.01.004
Xu Y, Wang Y-H, Liu T-Q, Zhang H, Zhang H, Li J (2018) The GlaA signal peptide substantially increases the expression and secretion of a-galactosidase in Aspergillus niger. Biotechnol Lett 40:949–955. https://doi.org/10.1007/s10529-018-2540-5
Yang S, Kuang Y, Li H, Liu Y, Hui X, Li P, Jiang Z, Zhou Y, Wang Y, Xu A, Li S, Liu P, Wu D (2013) Enhanced production of recombinant secretory proteins in Pichia pastoris by optimizing Kex2 P1’ site. PLoS ONE 8:e75347. https://doi.org/10.1371/journal.pone.0075347
Zhang B, Chen Y, Li Z, Lu W, Cao Y (2011) Cloning and functional expression of α-galactosidase cDNA from Penicillium janczewskii zaleski. Biologia (bratisl) 66:205–212. https://doi.org/10.2478/s11756-011-0014-5
Zhang J, Song G, Mei Y, Li R, Zhang H, Liu Y (2019) Present status on removal of raffinose family oligosaccharides—a review. Czech J Food Sci 37:141–154. https://doi.org/10.17221/472/2016-CJFS
Zhao R, Zhao R, Tu Y, Zhang X, Deng L, Chen X (2018) A novel α-galactosidase from the thermophilic probiotic Bacillus coagulans with remarkable protease-resistance and high hydrolytic activity. PLoS ONE 13:e0197067. https://doi.org/10.1371/journal.pone.0197067
Zheng X, Fang B, Han D, Yang W, Qi F, Chen H (2016) Improving the secretory expression of an -galactosidase from Aspergillus niger in Pichia pastoris. PLoS ONE 11:e0161529. https://doi.org/10.1371/journal.pone.0161529
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Anisha, G.S. Molecular advances in microbial α-galactosidases: challenges and prospects. World J Microbiol Biotechnol 38, 148 (2022). https://doi.org/10.1007/s11274-022-03340-2
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DOI: https://doi.org/10.1007/s11274-022-03340-2