Aspergillus oryzae α-l-rhamnosidase: Crystal structure and insight into the substrate specificity.

Aspergillus oryzae N-glycosylation Pichia pastoris crystal structure substrate specificity α-l-rhamnosidase

Journal

Proteins
ISSN: 1097-0134
Titre abrégé: Proteins
Pays: United States
ID NLM: 8700181

Informations de publication

Date de publication:
11 Oct 2023
Historique:
revised: 16 09 2023
received: 10 07 2023
accepted: 28 09 2023
medline: 11 10 2023
pubmed: 11 10 2023
entrez: 11 10 2023
Statut: aheadofprint

Résumé

The subsequent biochemical and structural investigations of the purified recombinant α-l-rhamnosidase from Aspergillus oryzae expressed in Pichia pastoris, designated as rAoRhaA, were performed. The specific activity of the rAoRhaA wild-type was higher toward hesperidin and narirutin, where the l-rhamnose residue was α-1,6-linked to β-d-glucoside, than toward neohesperidin and naringin with an α-1,2-linkage to β-d-glucoside. However, no activity was detected toward quercitrin, myricitrin, and epimedin C. rAoRhaA kinetic analysis indicated that K

Identifiants

pubmed: 37818702
doi: 10.1002/prot.26608
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : YU-COE Program of Yamagata University
Organisme : JSPS KAKENHI
ID : 22H01873

Informations de copyright

© 2023 Wiley Periodicals LLC.

Références

Williams PJ, Strauss CR, Wilson B. Classification of the monoterpenoid composition of Muscat grapes. Am J Enol Vitic. 1981;32:230-235.
Yanai T, Sato M. Purification and characterization of an α-L-rhamnosidase from Pichia angusta X349. Biosci Biotechnol Biochem. 2000;64:2179-2185.
Manzanares P, Orejas M, Gil JV, de Graaff LH, Visser J, Ramón D. Construction of a genetically modified wine yeast strain expressing the Aspergillus aculeatus rhaA gene, encoding an α-L-rhamnosidase of enological interest. Appl Environ Microbiol. 2003;69:7558-7562.
Maicas S, Mateo JJ. Hydrolysis of terpenyl glycoside in grape juice other fruit juices: a review. Appl Microbiol Biotechnol. 2005;67:322-335.
Yadav V, Yadav PK, Yadav S, Yadav KDS. α-L-Rhamnosidase: a review. Process Biochem. 2010;45:1226-1235.
González-Pombo P, Fariña L, Carrau F, Batista-Viera F, Brena BM. Aroma enhancement in wines using co-immobilized Aspergillus niger glycosidases. Food Chem. 2014;143:185-191.
Puri M, Marwaha SS, Kothari RM, Kennedy JF. Biochemical basis of bitterness in citrus fruit juices and biotech approaches for debittering. Crit Rev Biotechnol. 1996;16:145-155.
Yadav S, Yadav RSS, Yadav KDS. An α-L-rhamnosidase from Aspergillus awamori MTCC-2879 and its role in debittering of orange juice. Int J Food Sci Technol. 2013;48:927-933.
Hashimoto W, Miyake O, Nankai H, Murata K. Molecular identification of an α-L-rhamnosidase from Bacillus sp. strain GL1 as an enzyme involved in complete metabolism of gellan. Arch Biochem Biophys. 2003;415:235-244.
Pan L, Zhang Y, Zhang F, Wang Z, Zheng J. α-L-rhamnosidase: production, properties, and applications. World J Microbiol Biotechnol. 2023;39:191.
Manzanares P, van den Broeck HC, de Graaff LH, Visser J. Purification and characterization of two different α-L-rhamnosidases, RhaA and RhaB, from Aspergillus aculeatus. Appl Environ Microbiol. 2001;67:2230-2234.
Shanmugaprakash M, Vinothkumar V, Ragupathy J, Reddy DA. Biochemical characterization of three phase partitioned naringinase from Aspergillus brasiliensis MTCC 1344. Int J Biol Macromol. 2015;80:418-423.
Koseki T, Mese Y, Nishibori N, et al. Characterization of an alpha-L-rhamnosidase from Aspergillus kawachii and its gene. Appl Microbiol Biotechnol. 2008;80:1007-1013.
Ishikawa M, Shiono Y, Koseki T. Biochemical characterization of Aspergillus oryzae recombinant α-L-rhamnosidase expressed in Pichia pastoris. J Biosci Bioeng. 2017;124:630-634.
Tamayo-Ramos JA, Flipphi M, Pardo E, Manzanares P, Orejas M. L-rhamnose induction of Aspergillus nidulans α-L-rhamnosidase genes is glucose repressed via a CreA-independent mechanism acting at the level of inducer uptake. Microb Cell Fact. 2012;11:26.
Pardo E, Orejas M. The Aspergillus nidulans Zn(II)2Cys6 transcription factor AN5673/RhaR mediates L-rhamnose utilization and the production of α-L-rhamnosidases. Microb Cell Fact. 2014;13:161.
Lyu Y, Zeng W, Du G, Chen J, Zhou J. Efficient bioconversion of epimedin C to icariin by a glycosidase from Aspergillus nidulans. Bioresour Technol. 2019;289:121612.
Li L, Yu Y, Zhang X, et al. Expression and biochemical characterization of recombinant α-l-rhamnosidase r-Rha1 from Aspergillus Niger JMU-TS528. Int J Biol Macromol. 2016;85:391-399.
Spohner SC, Zahn D, Schaum V, Quitmann H, Czermak P. Recombinant α-L-rhamnosidase from Aspergillus terreus in selective trimming of α-L-rhamnose from steviol glycosides. J Mol Catal B: Enzym. 2015;122:248-254.
Li L, Gong J, Wang S, et al. Heterologous expression and characterization of a new clade of Aspergillus α-L-rhamnosidase suitable for citrus juice processing. J Agric Food Chem. 2019;67:2926-2935.
Bonanno JB, Almo SC, Bresnick A, et al. New York-Structural GenomiX Research Consortium (NYSGXRC): a large scale center for the protein structure initiative. J Struct Funct Genomics. 2005;6:225-232.
Cui Z, Maruyama Y, Mikami B, Hashimoto W, Murata K. Crystal structure of glycoside hydrolase family 78 alpha-L-rhamnosidase from Bacillus sp. GL1. J Mol Biol. 2007;374:384-398.
Fujimoto Z, Jackson A, Michikawa M, et al. The structure of a Streptomyces avermitilis α-L-rhamnosidase reveals a novel carbohydrate-binding module CBM67 within the six-domain arrangement. J Biol Chem. 2013;288:12376-12385.
O'Neill EC, Stevenson CE, Paterson MJ, et al. Crystal structure of a novel two domain GH78 family α-rhamnosidase from Klebsiella oxytoca with rhamnose bound. Proteins. 2015;83:1742-1749.
Pachl P, Škerlová J, Šimčíková D, et al. Crystal structure of native α-L-rhamnosidase from Aspergillus terreus. Acta Crystallogr Sect D Struct Biol. 2018;74(Pt 11):1078-1084.
Guillotin L, Kim H, Traore Y, et al. Biochemical characterization of the α-L-rhamnosidase DtRha from Dictyoglomus thermophilum: application to the selective derhamnosylation of natural flavonoids. ACS Omega. 2019;4:1916-1922.
Kaneko S, Fujimoto Z. α-L-Rhamnosidases: structures, substrate specificities, and their applications. Glycoside Hydrolases. Academic Press; 2023:349-364.
Kabsch WXDS. XDS. Acta Crystallogr Sect D Struct Biol. 2010;66:125-132.
Collaborative Computational Project Number 4. The CCP4 suite: programs for protein crystallography. Acta Crystallogr Sect D Struct Biol. 1994;50:760-763.
Baek M, Dimaio F, Anishchenko I, et al. Accurate prediction of protein structures and interactions using a three-track neural network. Science. 2021;373:871-876.
Adams PD, Afonine PV, Bunkóczi G, et al. PHENIX: a comprehensive python-based system for macromolecular structure solution. Acta Crystallogr Sect D Struct Biol. 2010;66:213-221.
Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D Struct Biol. 2004;60:2126-2132.
Chovancova E, Pavelka A, Benes P, et al. CAVER 3.0: a tool for the analysis of transport pathways in dynamic protein structures. PLoS Comput Biol. 2012;8:e1002708.
Holm L. Dali server: structural unification of protein families. Nucl Acids Res. 2022;50:W210-W215.
Manzanares P, Orejas M, Ibañez E, Vallés S, Ramón D. Purification and characterization of an α-L-rhamnosidase from Aspergillus nidulans. Lett Appl Microbiol. 2000;31:189-202.
Matsumoto S, Yamada H, Kunishige Y, et al. Identification of a novel Penicillium chrysogenum rhamnogalacturonan rhamnohydrolase and the first report of a rhamnogalacturonan rhamnohydrolase gene. Enzyme Microb Technol. 2017;98:76-85.
Yu B, Luo S, Ding Y, Gong Z, Nie T. Insights into glycosidic bond specificity of an engineered selective α-L-rhamnosidase N12-Rha via activity assays and molecular modelling. AMB Expr. 2022;12:143.
Wu T, Pei J, Ge L, et al. Characterization of a α-L-rhamnosidase from Bacteroides thetaiotaomicron with high catalytic efficiency of epimedin C. Bioorg Chem. 2018;81:461-467.
Xie J, Zhang S, Tong X, Wu T, Pei J, Zhao L. Biochemical characterization of a hyperthermophilic α-L-rhamnosidase from Thermotoga perrophila and its application in production of icaritin from epimedin C with a thermostable β-glucosidase. Process Biochem. 2020;93:115-124.
Ichinose H, Fujimoto Z, Kaneko S. Characterization of an α-L-rhamnosidase from Streptomyces avermitilis. Biosci Biotechnol Biochem. 2013;77:213-216.
Bauer S, Vasu P, Persson S, Mort AJ, Somerville CR. Development and application of a suite of polysaccharide-degrading enzymes for analyzing plant cell walls. Proc Natl Acad Sci U S A. 2006;103:11417-11422.
Pitson SM, Mutter M, van den Broek LA, Voragen AG, Beldman G. Stereochemical course of hydrolysis catalysed by alpha-L-rhamnosyl and alpha-D-galacturonosyl hydrolases from Aspergillus aculeatus. Biochem Biophys Res Commun. 1998;242:552-559.
Zverlov VV, Hertel C, Bronnenmeier K, Hroch A, Kellermann J, Schwarz WH. The thermostable alpha-L-rhamnosidase RamA of Clostridium stercorarium: biochemical characterization and primary structure of a bacterial alpha-L-rhamnoside hydrolase, a new type of inverting glycoside hydrolase. Mol Microbiol. 2000;35:173-179.

Auteurs

Koki Makabe (K)

Graduate School of Science and Engineering, Faculty of Engineering, Yamagata University, Yonezawa, Japan.

Naoki Ishida (N)

Department of Food, Life and Environmental Sciences, Faculty of Agriculture, Yamagata University, Tsuruoka, Japan.

Nanako Kanezaki (N)

Department of Food, Life and Environmental Sciences, Faculty of Agriculture, Yamagata University, Tsuruoka, Japan.

Yoshihito Shiono (Y)

Department of Food, Life and Environmental Sciences, Faculty of Agriculture, Yamagata University, Tsuruoka, Japan.

Takuya Koseki (T)

Department of Food, Life and Environmental Sciences, Faculty of Agriculture, Yamagata University, Tsuruoka, Japan.

Classifications MeSH