The many functions of carbohydrate-active enzymes in family GH65: diversity and application.
Carbohydrate-active enzymes
Glycoside Hydrolase family 65
Glycoside hydrolases
Glycoside phosphorylases
Glycosyltransferases
One-pot cascade reactions
Specificity determinants
Journal
Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612
Informations de publication
Date de publication:
30 Sep 2024
30 Sep 2024
Historique:
received:
19
07
2024
accepted:
30
08
2024
revised:
29
08
2024
medline:
30
9
2024
pubmed:
30
9
2024
entrez:
30
9
2024
Statut:
epublish
Résumé
Glycoside Hydrolase family 65 (GH65) is a unique family of carbohydrate-active enzymes. It is the first protein family to bring together glycoside hydrolases, glycoside phosphorylases and glycosyltransferases, thereby spanning a broad range of reaction types. These enzymes catalyze the hydrolysis, reversible phosphorolysis or synthesis of various α-glucosides, typically α-glucobioses or their derivatives. In this review, we present a comprehensive overview of the diverse reaction types and substrate specificities found in family GH65. We describe the determinants that control this remarkable diversity, as well as the applications of GH65 enzymes for carbohydrate synthesis.
Identifiants
pubmed: 39348028
doi: 10.1007/s00253-024-13301-4
pii: 10.1007/s00253-024-13301-4
doi:
Substances chimiques
Glycoside Hydrolases
EC 3.2.1.-
Glycosyltransferases
EC 2.4.-
Phosphorylases
EC 2.4.1.-
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
476Subventions
Organisme : Research Foundation Flanders (FWO) (BE)
ID : 1S17721N
Informations de copyright
© 2024. The Author(s).
Références
Alizadeh P, Klionsky DJ (1996) Purification and biochemical characterization of the ATH1 gene product, vacuolar acid trehalase, from Saccharomyces cerevisiae FEBS Lett 391:273–278. https://doi.org/10.1016/0014-5793(96)00751-X
doi: 10.1016/0014-5793(96)00751-X
pubmed: 8764988
Andersen S, Møller MS, Poulsen J-CN, Pichler MJ, Svensson B, Lo Leggio L, Goh YJ, Abou Hachem M (2020) An 1,4-α-Glucosyltransferase defines a new maltodextrin catabolism scheme in Lactobacillus acidophilus. Appl Environ Microbiol 86:e00661–e00620. https://doi.org/10.1128/AEM.00661-20
doi: 10.1128/AEM.00661-20
pubmed: 32444471
pmcid: 7376546
Andersson U, Levander F, Rådström P (2001) Trehalose-6-phosphate phosphorylase is part of a novel metabolic pathway for trehalose utilization in Lactococcus lactis. J Biol Chem 276:42707–42713. https://doi.org/10.1074/jbc.M108279200
doi: 10.1074/jbc.M108279200
pubmed: 11553642
Awad FN (2021) Glycoside phosphorylases for carbohydrate synthesis: an insight into the diversity and potentiality. Biocatal Agric Biotechnol 31:101886. https://doi.org/10.1016/j.bcab.2020.101886
doi: 10.1016/j.bcab.2020.101886
Bi R, Wu J, Su L, Xia W (2022) Efficient synthesis of nigerose by a novel nigerose phosphorylase from Anaerosporobacter mobilis Syst Microbiol Biomanuf 1:1–11. https://doi.org/10.1007/S43393-022-00122-7
doi: 10.1007/S43393-022-00122-7
Chaen H, Nakada T, Nishimoto T, Kuroda N, Fukuda S, Sugimoto T, Kurimoto M, Yoshio T (1999a) Purification and characterization of thermostable trehalose phosphorylase from Thermoanaerobium brockii J Appl Glycosci 46:399–405. https://doi.org/10.5458/jag.46.399
doi: 10.5458/jag.46.399
Chaen H, Yamamoto T, Nishimoto T, Nakada T, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y (1999b) Purification and characterization of a novel phosphorylase, kojibiose phosphorylase, from Thermoanaerobium brockii. J Appl Glycosci 46:423–429. https://doi.org/10.5458/jag.46.423
doi: 10.5458/jag.46.423
Chaen H, Nakada T, Mukai N, Nishimoto T, Fukuda S, Sugimoto T, Kurimoto M, Tsujisaka Y (2001a) Efficient enzymatic synthesis of disaccharide, α-D-galactosyl α-D-glucoside, by trehalose phosphorylase from Thermoanaerobacter brockii J Appl Glycosci 48:135–137. https://doi.org/10.5458/jag.48.135
doi: 10.5458/jag.48.135
Chaen H, Nishimoto T, Nakada T, Fukuda S, Kurimoto M, Tsujisaka Y (2001b) Enzymatic synthesis of kojioligosaccharides using kojibiose phosphorylase. J Biosci Bioeng 92:177–182. https://doi.org/10.1016/S1389-1723(01)80221-8
doi: 10.1016/S1389-1723(01)80221-8
pubmed: 16233080
Chen C, Van Der Borght J, De Vreese R, D’Hooghe M, Soetaert W, Desmet T (2014) Engineering the specificity of trehalose phosphorylase as a general strategy for the production of glycosyl phosphates. Chem Commun 50:7834–7836. https://doi.org/10.1039/c4cc02202e
doi: 10.1039/c4cc02202e
Curiel JA, Peirotén Á, Landete JM, Ruiz de la Bastida A, Langa S, Arqués JL (2021) Architecture insight of bifidobacterial α-L-fucosidases. Int J Mol Sci 22:8462. https://doi.org/10.3390/ijms22168462
doi: 10.3390/ijms22168462
pubmed: 34445166
pmcid: 8395109
D’Enfert C, Fontaine T (1997) Molecular characterization of the Aspergillus nidulans treA gene encoding an acid trehalase required for growth on trehalose. Mol Microbiol 24:203–216. https://doi.org/10.1046/j.1365-2958.1997.3131693.x
doi: 10.1046/j.1365-2958.1997.3131693.x
pubmed: 9140977
Davies GJ, Wilson KS, Henrissat B (1997) Nomenclature for sugar-binding subsites in glycosyl hydrolases. Biochem J 321:557–559. https://doi.org/10.1042/bj3210557
De Beul E, Jongbloet A, Franceus J, Desmet T (2021) Discovery of a kojibiose hydrolase by analysis of specificity-determining correlated positions in Glycoside Hydrolase family 65. Molecules 26:6321. https://doi.org/10.3390/MOLECULES26206321
doi: 10.3390/MOLECULES26206321
pubmed: 34684901
pmcid: 8537180
Desmet T, Soetaert W (2011) Enzymatic glycosyl transfer: mechanisms and applications. Biocatal Biotransform 29:1–18. https://doi.org/10.3109/10242422.2010.548557
doi: 10.3109/10242422.2010.548557
Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B, Terrapon N (2022) The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 50:D571–D577. https://doi.org/10.1093/nar/gkab1045
doi: 10.1093/nar/gkab1045
pubmed: 34850161
Egloff MP, Uppenberg J, Haalck L, van Tilbeurgh H (2001) Crystal structure of maltose phosphorylase from Lactobacillus brevis: unexpected evolutionary relationship with glucoamylases. Structure 9:689–697. https://doi.org/10.1016/S0969-2126(01)00626-8
doi: 10.1016/S0969-2126(01)00626-8
pubmed: 11587643
Ehrmann MA, Vogel RF (1998) Maltose metabolism of Lactobacillus sanfranciscensis: cloning and heterologous expression of the key enzymes, maltose phosphorylase and phosphoglucomutase. FEMS Microbiol Lett 169:81–86. https://doi.org/10.1111/j.1574-6968.1998.tb13302.x
doi: 10.1111/j.1574-6968.1998.tb13302.x
pubmed: 9851037
Franceus J, Desmet T (2020) Sucrose phosphorylase and related enzymes in Glycoside Hydrolase family 13: discovery, application and engineering. Int J Mol Sci 21:2526. https://doi.org/10.3390/ijms21072526
doi: 10.3390/ijms21072526
pubmed: 32260541
pmcid: 7178133
Franceus J, Verhaeghe T, Desmet T (2017) Correlated positions in protein evolution and engineering. J Ind Microbiol Biotechnol 44:687–695. https://doi.org/10.1007/s10295-016-1811-1
doi: 10.1007/s10295-016-1811-1
pubmed: 27514664
Franceus J, Decuyper L, D’hooghe M, Desmet T (2018) Exploring the sequence diversity in glycoside hydrolase family 13_18 reveals a novel glucosylglycerol phosphorylase. Appl Microbiol Biotechnol 102:3183–3191. https://doi.org/10.1007/s00253-018-8856-1
doi: 10.1007/s00253-018-8856-1
pubmed: 29470619
Franceus J, Lormans J, Cools L, D’hooghe M, Desmet T (2021) Evolution of phosphorylases from N-acetylglucosaminide hydrolases in family GH3. ACS Catal 11:6225–6233. https://doi.org/10.1021/ACSCATAL.1C00761
doi: 10.1021/ACSCATAL.1C00761
Franceus J, Lormans J, Desmet T (2022) Building mutational bridges between carbohydrate-active enzymes. Curr Opin Biotechnol 78:102804. https://doi.org/10.1016/j.copbio.2022.102804
doi: 10.1016/j.copbio.2022.102804
pubmed: 36156353
Franceus J, Rivas-Fernández JP, Lormans J, Rovira C, Desmet T (2024) Evolution of phosphorylase activity in an ancestral glycosyltransferase. ACS Catal 14:3103–3114. https://doi.org/10.1021/acscatal.3c05819
doi: 10.1021/acscatal.3c05819
pubmed: 38449530
pmcid: 10913872
Fujinaka H, Nakamura J, Murase D, Souno H, Kobayashi H (2004) Sugar phosphates and their use for improving the intestinal function. European Patent 1477173A1
Fujinaka H, Nakamura J, Kobayashi H, Takizawa M, Murase D, Tokimitsu I, Suda T (2007) Glucose 1-phosphate increases active transport of calcium in intestine. Arch Biochem Biophys 460:152–160. https://doi.org/10.1016/j.abb.2006.09.006
doi: 10.1016/j.abb.2006.09.006
pubmed: 17320035
Gao Y, Saburi W, Taguchi Y, Mori H (2019) Biochemical characteristics of maltose phosphorylase MalE from Bacillus sp. AHU2001 and chemoenzymatic synthesis of oligosaccharides by the enzyme. Biosci Biotechnol Biochem 83:2097–2109. https://doi.org/10.1080/09168451.2019.1634516
doi: 10.1080/09168451.2019.1634516
pubmed: 31262243
Gu J, Xu Y, Nie Y (2023) Role of distal sites in enzyme engineering. Biotechnol Adv 63:108094. https://doi.org/10.1016/j.biotechadv.2023.108094
doi: 10.1016/j.biotechadv.2023.108094
pubmed: 36621725
Hamazaki H, Hamazaki MH (2016) Catalytic site of human protein-glucosylgalactosylhydroxylysine glucosidase: three crucial carboxyl residues were determined by cloning and site-directed mutagenesis. Biochem Biophys Res Commun 469:357–362. https://doi.org/10.1016/j.bbrc.2015.12.005
doi: 10.1016/j.bbrc.2015.12.005
pubmed: 26682924
Hamazaki H, Hotta K (1979) Purification and characterization of an α-glucosidase specific for hydroxylysine-linked disaccharide of collagen. J Biol Chem 254:9682–9687. https://doi.org/10.1016/s0021-9258(19)83570-6
doi: 10.1016/s0021-9258(19)83570-6
pubmed: 385589
Hidaka M, Honda Y, Kitaoka M, Nirasawa S, Hayashi K, Wakagi T, Shoun H, Fushinobu S (2004) Chitobiose phosphorylase from Vibrio proteolyticus, a member of Glycosyl Transferase family 36, has a clan GH-L-like (α/α)
doi: 10.1016/j.str.2004.03.027
pubmed: 15274915
Hidaka Y, Hatada Y, Akita M, Yoshida M, Nakamura N, Takada M, Nakakuki T, Ito S, Horikoshi K (2005) Maltose phosphorylase from a deep-sea Paenibacillus sp.: enzymatic properties and nucleotide and amino-acid sequences. Enzyme Microb Technol 37:185–194. https://doi.org/10.1016/j.enzmictec.2005.02.010
doi: 10.1016/j.enzmictec.2005.02.010
Huang Y, Niu B, Gao Y, Fu L, Li W (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26:680–682. https://doi.org/10.1093/BIOINFORMATICS/BTQ003
doi: 10.1093/BIOINFORMATICS/BTQ003
pubmed: 20053844
pmcid: 2828112
Hüwel S, Haalck L, Conrath N, Spener F (1997) Maltose phosphorylase from Lactobacillus brevis: purification, characterization, and application in a biosensor for ortho-phosphate. Enzyme Microb Technol 21:413–420. https://doi.org/10.1016/S0141-0229(97)00014-8
doi: 10.1016/S0141-0229(97)00014-8
pubmed: 9343859
Inoue Y, Ishii K, Tomita T, Yatake T, Fukui F (2002a) Characterization of trehalose phosphorylase from Bacillus stearothermophilus SK-1 and nucleotide sequence of the corresponding gene. Biosci Biotechnol Biochem 66:1835–1843. https://doi.org/10.1271/bbb.66.1835
doi: 10.1271/bbb.66.1835
pubmed: 12400680
Inoue Y, Yasutake N, Oshima Y, Yamamoto Y, Tomita T, Miyoshi S, Yatake T (2002b) Cloning of the maltose phosphorylase gene from Bacillus sp. strain RK-1 and efficient production of the cloned gene and the trehalose phosphorylase gene from Bacillus stearothermophilus SK-1 in Bacillus subtilis. Biosci Biotechnol Biochem 66:2594–2599. https://doi.org/10.1271/bbb.66.2594
doi: 10.1271/bbb.66.2594
pubmed: 12596853
Isono N, Yagura S, Yamanaka K, Masuda Y, Mukai K, Katsuzaki H (2023) Enzymatic synthesis of β-D-fructofuranosyl α-D-glucopyranosyl-(1→2)-α-D-glucopyranoside using Escherichia coli glycoside phosphorylase YcjT. Biosci Biotechnol Biochem 87:1249–1253. https://doi.org/10.1093/bbb/zbad099
doi: 10.1093/bbb/zbad099
pubmed: 37475702
Jung JH, Seo DH, Holden JF, Park CS (2014) Identification and characterization of an archaeal kojibiose catabolic pathway in the hyperthermophilic Pyrococcus sp. strain ST04. J Bacteriol 196:1122–1131. https://doi.org/10.1128/JB.01222-13
doi: 10.1128/JB.01222-13
pubmed: 24391053
pmcid: 3957703
Kabisch A, Otto A, König S, Becher D, Albrecht D, Schüler M, Teeling H, Amann RI, Schweder T (2014) Functional characterization of polysaccharide utilization loci in the marine Bacteroidetes ‘Gramella Forsetii’ KT0803. ISME J 8:1492–1502. https://doi.org/10.1038/ismej.2014.4
doi: 10.1038/ismej.2014.4
pubmed: 24522261
pmcid: 4069401
Kamogawa A, Yokobayashi K, Fukui T (1973) Properties of maltose phosphorylase from Lactobacillus brevis Agric Biol Chem 37:2813–2819. https://doi.org/10.1271/bbb1961.37.2813
doi: 10.1271/bbb1961.37.2813
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
doi: 10.1093/bib/bbx108
pubmed: 28968734
Kido Y, Maeno S, Tanno H, Kichise Y, Shiwa Y, Endo A (2021) Niche-specific adaptation of Lactobacillus helveticus strains isolated from malt whisky and dairy fermentations. Microb Genomics 7:000560. https://doi.org/10.1099/mgen.0.000560
doi: 10.1099/mgen.0.000560
Kuhaudomlarp S, Pergolizzi G, Patron NJ, Henrissat B, Field RA (2019) Unraveling the subtleties of β-(1→3)-glucan phosphorylase specificity in the GH94, GH149, and GH161 glycoside hydrolase families. J Biol Chem 294:6483–6493. https://doi.org/10.1074/jbc.RA119.007712
doi: 10.1074/jbc.RA119.007712
pubmed: 30819804
pmcid: 6484121
La Rosa SL, Leth ML, Michalak L, Hansen ME, Pudlo NA, Glowacki R, Pereira G, Workman CT, Arntzen MØ, Pope PB, Martens EC, Hachem MA, Westereng B (2019) The human gut Firmicute Roseburia intestinalis is a primary degrader of dietary β-mannans. Nat Commun 10:905. https://doi.org/10.1038/s41467-019-08812-y
doi: 10.1038/s41467-019-08812-y
pubmed: 30796211
pmcid: 6385246
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296. https://doi.org/10.1093/NAR/GKAB301
doi: 10.1093/NAR/GKAB301
pubmed: 33885785
pmcid: 8265157
Li A, Laville E, Tarquis L, Lombard V, Ropartz D, Terrapon N, Henrissat B, Guieysse D, Esque J, Durand J, Morgavi DP, Potocki-Veronese G (2020) Analysis of the diversity of the glycoside hydrolase family 130 in mammal gut microbiomes reveals a novel mannoside-phosphorylase function. Microb Genomics 6:1–14. https://doi.org/10.1099/mgen.0.000404
doi: 10.1099/mgen.0.000404
Li A, Benkoulouche M, Ladeveze S, Durand J, Cioci G, Laville E, Potocki-Veronese G (2022) Discovery and biotechnological exploitation of glycoside-phosphorylases. Int J Mol Sci 23:3043. https://doi.org/10.3390/ijms23063043
doi: 10.3390/ijms23063043
pubmed: 35328479
pmcid: 8950772
Liu Y, Wang Z, Yin Y, Cao Y, Zhao H, Xia Y (2007) Expression, purification, and characterization of recombinant Metarhizium anisopliae acid trehalase in Pichia pastoris. Protein Expr Purif 54:66–72. https://doi.org/10.1016/j.pep.2007.02.016
doi: 10.1016/j.pep.2007.02.016
pubmed: 17419071
Liu N, Fosses A, Kampik C, Parsiegla G, Denis Y, Vita N, Fierobe H-P, Perret S (2019) In vitro and in vivo exploration of the cellobiose and cellodextrin phosphorylases panel in Ruminiclostridium cellulolyticum: implication for cellulose catabolism. Biotechnol Biofuels 12:208. https://doi.org/10.1186/s13068-019-1549-x
doi: 10.1186/s13068-019-1549-x
pubmed: 31497068
pmcid: 6720390
Luley-Goedl C, Nidetzky B (2010) Carbohydrate synthesis by disaccharide phosphorylases: reactions, catalytic mechanisms and application in the glycosciences. Biotechnol J 5:1324–1338. https://doi.org/10.1002/biot.201000217
doi: 10.1002/biot.201000217
pubmed: 21154671
Maruta K, Mukai K, Yamashita H, Kubota M, Chaen H, Fukuda S, Kurimoto M (2002) Gene encoding a trehalose phosphorylase from Thermoanaerobacter brockii ATCC 35047. Biosci Biotechnol Biochem 66:1976–1980. https://doi.org/10.1271/bbb.66.1976
doi: 10.1271/bbb.66.1976
pubmed: 12400703
Maruta K, Watanabe H, Nishimoto T, Kubota M, Chaen H, Fukuda S, Kurimoto M, Tsujisaka Y (2006) Acceptor specificity of trehalose phosphorylase from Thermoanaerobacter brockii: production of novel nonreducing trisaccharide, 6-O-α-D-galactopyranosyl trehalose. J Biosci Bioeng 101:385–390. https://doi.org/10.1263/JBB.101.385
doi: 10.1263/JBB.101.385
pubmed: 16781466
Mittenbuhler K, Holzer H (1988) Purification and characterization of acid trehalase from the yeast suc2 mutant. J Biol Chem 263:8537–8543. https://doi.org/10.1016/s0021-9258(18)68511-4
doi: 10.1016/s0021-9258(18)68511-4
pubmed: 3286651
Miyazaki T, Park EY (2020) Structure–function analysis of silkworm sucrose hydrolase uncovers the mechanism of substrate specificity in GH13 subfamily 17 exo-α-glucosidases. J Biol Chem 295:8784–8797. https://doi.org/10.1074/jbc.RA120.013595
doi: 10.1074/jbc.RA120.013595
pubmed: 32381508
Miyazaki T, Tanaka H, Nakamura S, Dohra H, Funane K (2022) Identification and characterization of dextran α-1,2-debranching enzyme from Microbacterium dextranolyticum. J Appl Glycosci 70:15–24. https://doi.org/10.5458/jag.jag.JAG-2022_0013
doi: 10.5458/jag.jag.JAG-2022_0013
Mokhtari A, Blancato VS, Repizo GD, Henry C, Pikis A, Bourand A, de Fátima Álvarez M, Immel S, Mechakra-Maza A, Hartke A, Thompson J, Magni C, Deutscher J (2013) Enterococcus faecalis utilizes maltose by connecting two incompatible metabolic routes via a novel maltose 6′-phosphate phosphatase (MapP). Mol Microbiol 88:234–253. https://doi.org/10.1111/mmi.12183
doi: 10.1111/mmi.12183
pubmed: 23490043
pmcid: 3633101
Mukherjee K, Narindoshvili T, Raushel FM (2018) Discovery of a kojibiose phosphorylase in Escherichia coli K-12. Biochemistry 57:2857–2867. https://doi.org/10.1021/acs.biochem.8b00392
doi: 10.1021/acs.biochem.8b00392
pubmed: 29684280
Murao S, Nagano H, Ogura S, Nishino T (1985) Enzymatic synthesis of trehalose from maltose. Agric Biol Chem 49:2113–2118. https://doi.org/10.1271/bbb1961.49.2113
doi: 10.1271/bbb1961.49.2113
Nakai H, Baumann MJ, Petersen BO, Westphal Y, Schols H, Dilokpimol A, Hachem MA, Lahtinen SJ, Duus JØ, Svensson B (2009) The maltodextrin transport system and metabolism in Lactobacillus acidophilus NCFM and production of novel α-glucosides through reverse phosphorolysis by maltose phosphorylase. FEBS J 276:7353–7365. https://doi.org/10.1111/j.1742-4658.2009.07445.x
doi: 10.1111/j.1742-4658.2009.07445.x
pubmed: 19919544
Nakai H, Dilokpimol A, Hachem MA, Svensson B (2010a) Efficient one-pot enzymatic synthesis of α-(1→4)-glucosidic disaccharides through a coupled reaction catalysed by Lactobacillus acidophilus NCFM maltose phosphorylase. Carbohydr Res 345:1061–1064. https://doi.org/10.1016/j.carres.2010.03.021
doi: 10.1016/j.carres.2010.03.021
pubmed: 20392438
Nakai H, Petersen BO, Westphal Y, Dilokpimol A, Abou Hachem M, Duus JØ, Schols HA, Svensson B (2010b) Rational engineering of Lactobacillus acidophilus NCFM maltose phosphorylase into either trehalose or kojibiose dual specificity phosphorylase. Protein Eng Des Sel 23:781–787. https://doi.org/10.1093/protein/gzq055
doi: 10.1093/protein/gzq055
pubmed: 20713411
Nakamura S, Nihira T, Kurata R, Nakai H, Funane K, Park EY, Miyazaki T (2021) Structure of a bacterial α-1,2-glucosidase defines mechanisms of hydrolysis and substrate specificity in GH65 family hydrolases. J Biol Chem 297:101366. https://doi.org/10.1016/J.JBC.2021.101366
doi: 10.1016/J.JBC.2021.101366
pubmed: 34728215
pmcid: 8626586
Nakamura S, Kurata R, Miyazaki T (2024) Structural insights into α-(1→6)-linkage preference of GH97 glucodextranase from Flavobacterium johnsoniae FEBS J. https://doi.org/10.1111/febs.17139
doi: 10.1111/febs.17139
pubmed: 39073006
Nihira T, Nakai H, Chiku K, Kitaoka M (2012a) Discovery of nigerose phosphorylase from Clostridium phytofermentans Appl Microbiol Biotechnol 93:1513–1522. https://doi.org/10.1007/s00253-011-3515-9
doi: 10.1007/s00253-011-3515-9
pubmed: 21808968
Nihira T, Nakai H, Kitaoka M (2012b) 3-O-α-D-glucopyranosyl-L-rhamnose phosphorylase from Clostridium phytofermentans Carbohydr Res 350:94–97. https://doi.org/10.1016/j.carres.2011.12.019
doi: 10.1016/j.carres.2011.12.019
pubmed: 22277537
Nihira T, Saito Y, Kitaoka M, Otsubo K, Nakai H (2012c) Identification of Bacillus selenitireducens MLS10 maltose phosphorylase possessing synthetic ability for branched α-D-glucosyl trisaccharides. Carbohydr Res 360:25–30. https://doi.org/10.1016/j.carres.2012.07.014
doi: 10.1016/j.carres.2012.07.014
pubmed: 22940176
Nihira T, Saito Y, Chiku K, Kitaoka M, Ohtsubo K, Nakai H (2013) Potassium ion-dependent trehalose phosphorylase from halophilic Bacillus selenitireducens MLS10. FEBS Lett 587:3382–3386. https://doi.org/10.1016/j.febslet.2013.08.038
doi: 10.1016/j.febslet.2013.08.038
pubmed: 24021648
Nihira T, Miyajima F, Chiku K, Nishimoto M, Kitaoka M, Ohtsubo K, Nakai H (2014a) One pot enzymatic production of nigerose from common sugar resources employing nigerose phosphorylase. J Appl Glycosci 61:75–80. https://doi.org/10.5458/jag.jag.JAG-2013_012
doi: 10.5458/jag.jag.JAG-2013_012
Nihira T, Nishimoto M, Nakai H, Ohtsubo K, Kitaoka M (2014b) Characterization of two α-1,3-glucoside phosphorylases from Clostridium phytofermentans. J Appl Glycosci 61:59–66. https://doi.org/10.5458/jag.jag.JAG-2013_013
doi: 10.5458/jag.jag.JAG-2013_013
Nihira T, Saito Y, Ohtsubo K, Nakai H, Kitaoka M (2014c) 2-O-α-D-Glucosylglycerol phosphorylase from Bacillus selenitireducens MLS10 possessing hydrolytic activity on β-D-glucose 1-phosphate. PLoS ONE 9:e86548. https://doi.org/10.1371/journal.pone.0086548
doi: 10.1371/journal.pone.0086548
pubmed: 24466148
pmcid: 3899277
Okada S, Yamamoto T, Watanabe H, Nishimoto T, Chaen H, Fukuda S, Wakagi T, Fushinobu S (2014) Structural and mutational analysis of substrate recognition in kojibiose phosphorylase. FEBS J 281:778–786. https://doi.org/10.1111/febs.12622
doi: 10.1111/febs.12622
pubmed: 24255995
Osuna S (2021) The challenge of predicting distal active site mutations in computational enzyme design. WIREs Comput Mol Sci 11:e1502. https://doi.org/10.1002/wcms.1502
doi: 10.1002/wcms.1502
Parish CR, Cowden WB, Willenborg DO (1992) Phosphosugar-based anti-inflammatory and/or immunosuppressive drugs. US005506210A
Pedreño Y, Maicas S, Argüelles JC, Sentandreu R, Valentin E (2004) The ATC1 gene encodes a cell wall-linked acid trehalase required for growth on trehalose in Candida albicans J Biol Chem 279:40852–40860. https://doi.org/10.1074/jbc.M400216200
doi: 10.1074/jbc.M400216200
pubmed: 15252058
Plante OJ, Andrade RB, Seeberger PH (1999) Synthesis and use of glycosyl phosphates as glycosyl donors. Org Lett 1:211–214. https://doi.org/10.1021/ol9905452
doi: 10.1021/ol9905452
pubmed: 10905866
Price MN, Dehal PS, Arkin AP (2010) FastTree 2 - approximately maximum-likelihood trees for large alignments. PLoS ONE 5:e9490. https://doi.org/10.1371/journal.pone.0009490
doi: 10.1371/journal.pone.0009490
pubmed: 20224823
pmcid: 2835736
Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42:W320–W324. https://doi.org/10.1093/nar/gku316
doi: 10.1093/nar/gku316
pubmed: 24753421
pmcid: 4086106
Ronchera-Oms CL, Jiménez NV, Peidro J (1995) Stability of parenteral nutrition admixtures containing organic phosphates. Clin Nutr 14:373–380. https://doi.org/10.1016/S0261-5614(95)80055-7
doi: 10.1016/S0261-5614(95)80055-7
pubmed: 16843959
Sakaguchi M (2020) Diverse and common features of trehalases and their contributions to microbial trehalose metabolism. Appl Microbiol Biotechnol 104:1837–1847. https://doi.org/10.1007/s00253-019-10339-7
doi: 10.1007/s00253-019-10339-7
pubmed: 31925485
Sánchez-Fresneda R, Martínez-Esparza M, Maicas S, Argüelles J-C, Valentín E (2014) In Candida parapsilosis the ATC1 gene encodes for an acid trehalase involved in trehalose hydrolysis, stress resistance and virulence. PLoS One 9:e99113. https://doi.org/10.1371/journal.pone.0099113
Sánchez-Fresneda R, Guirao-Abad JP, Martinez-Esparza M, Maicas S, Valentín E, Argüelles J-C (2015) Homozygous deletion of ATC1 and NTC1 genes in Candida parapsilosis abolishes trehalase activity and affects cell growth, sugar metabolism, stress resistance, infectivity and biofilm formation. Fungal Genet Biol 85:45–57. https://doi.org/10.1016/j.fgb.2015.10.007
doi: 10.1016/j.fgb.2015.10.007
pubmed: 26529381
Sato S, Fan P-H, Yeh Y-C, Liu H (2024) Complete in vitro reconstitution of the apramycin biosynthetic pathway demonstrates the unusual incorporation of a β-D-sugar nucleotide in the final glycosylation step. J Am Chem Soc 146:10103–10114. https://doi.org/10.1021/jacs.4c01233
doi: 10.1021/jacs.4c01233
pubmed: 38546392
pmcid: 11317085
Sernee MF, Ralton JE, Nero TL, Sobala LF, Kloehn J, Vieira-Lara MA, Cobbold SA, Stanton L, Pires DEV, Hanssen E, Males A, Ward T, Bastidas LM, Van Der Peet PL, Parker MW, Ascher DB, Williams SJ, Davies GJ, McConville MJ (2019) A family of dual-activity glycosyltransferase-phosphorylases mediates mannogen turnover and virulence in Leishmania Parasites. Cell Host Microbe 26:385-399e9. https://doi.org/10.1016/j.chom.2019.08.009
doi: 10.1016/j.chom.2019.08.009
pubmed: 31513773
Shrestha P, Karmacharya J, Han S-R, Lee JH, Oh T-J (2023) Elucidation of bacterial trehalose-degrading trehalase and trehalose phosphorylase: physiological significance and its potential applications. Glycobiology 00:1–13. https://doi.org/10.1093/glycob/cwad084
doi: 10.1093/glycob/cwad084
Sigg A, Klimacek M, Nidetzky B (2024) Pushing the boundaries of phosphorylase cascade reaction for cellobiose production I: kinetic model development. Biotechnol Bioeng 121:580–592. https://doi.org/10.1002/bit.28602
doi: 10.1002/bit.28602
pubmed: 37983971
Sun S, You C (2021) Disaccharide phosphorylases: structure, catalytic mechanisms and directed evolution. Synth Syst Biotechnol 6:23–31. https://doi.org/10.1016/j.synbio.2021.01.004
doi: 10.1016/j.synbio.2021.01.004
pubmed: 33665389
pmcid: 7896129
Taguchi Y, Saburi W, Imai R, Mori H (2017) Evaluation of acceptor selectivity of Lactococcus lactis ssp. lactis trehalose 6-phosphate phosphorylase in the reverse phosphorolysis and synthesis of a new sugar phosphate. Biosci Biotechnol Biochem 81:1512–1519. https://doi.org/10.1080/09168451.2017.1329620
Taguchi Y, Saburi W, Imai R, Mori H (2020) Efficient one-pot enzymatic synthesis of trehalose 6-phosphate using GH65 α-glucoside phosphorylases. Carbohydr Res 488:107902. https://doi.org/10.1016/j.carres.2019.107902
doi: 10.1016/j.carres.2019.107902
pubmed: 31911362
Thibodeaux CJ, Melançon CE III, Liu H (2008) Natural-product sugar biosynthesis and enzymatic glycodiversification. Angew Chem Int Ed 47:9814–9859. https://doi.org/10.1002/anie.200801204
doi: 10.1002/anie.200801204
Touhara KK, Nihira T, Kitaoka M, Nakai H, Fushinobu S (2014) Structural basis for reversible phosphorolysis and hydrolysis reactions of 2-O-α-glucosylglycerol phosphorylase. J Biol Chem 289:18067–18075. https://doi.org/10.1074/jbc.M114.573212
doi: 10.1074/jbc.M114.573212
pubmed: 24828502
Van der Borght J, Desmet T, Soetaert W (2010) Enzymatic production of β-D-glucose-1-phosphate from trehalose. Biotechnol J 5:986–993. https://doi.org/10.1002/biot.201000203
doi: 10.1002/biot.201000203
pubmed: 20799297
Van der Borght J, Chen C, Hoflack L, Van Renterghem L, Desmet T, Soetaert W (2011) Enzymatic properties and substrate specificity of the trehalose phosphorylase from Caldanaerobacter subterraneus Appl Environ Microbiol 77:6939–6944. https://doi.org/10.1128/AEM.05190-11
doi: 10.1128/AEM.05190-11
pubmed: 21803886
pmcid: 3187076
Van der Borght J, Soetaert W, Desmet T (2012) Engineering the acceptor specificity of trehalose phosphorylase for the production of trehalose analogs. Biotechnol Prog 28:1257–1262. https://doi.org/10.1002/btpr.1609
doi: 10.1002/btpr.1609
pubmed: 22848048
Van Hoorebeke A, Stout J, Van der Meeren R, Kyndt J, Van Beeumen J, Savvides SN (2010) Crystallization and X-ray diffraction studies of inverting trehalose phosphorylase from Thermoanaerobacter Sp. Acta Crystallograph Sect F Struct Biol Cryst Commun 66:442–447. https://doi.org/10.1107/S1744309110005749
doi: 10.1107/S1744309110005749
Weinstock KG, Bush D (1999) Nucleic acid sequences relating to Candida albicans for diagnostics and therapeutics. US Patent 6747137B1
Wilding M, Hong N, Spence M, Buckle AM, Jackson CJ (2019) Protein engineering: the potential of remote mutations. Biochem Soc Trans 47:701–711. https://doi.org/10.1042/BST20180614
doi: 10.1042/BST20180614
pubmed: 30902926
Yamamoto T, Maruta K, Mukai K, Yamashita H, Nishimoto T, Kubota M, Fukuda S, Kurimoto M, Tsujisaka Y (2004) Cloning and sequencing of kojibiose phosphorylase gene from Thermoanaerobacter brockii ATCC35047. J Biosci Bioeng 98:99–106. https://doi.org/10.1016/s1389-1723(04)70249-2
doi: 10.1016/s1389-1723(04)70249-2
pubmed: 16233673
Yamamoto T, Watanabe H, Nishimoto T, Aga H, Kubota M, Chaen H, Fukuda S (2006a) Acceptor recognition of kojibiose phosphorylase from Thermoanaerobacter brockii: syntheses of glycosyl glycerol and myo-inositol. J Biosci Bioeng 101:427–433. https://doi.org/10.1263/jbb.101.427
doi: 10.1263/jbb.101.427
pubmed: 16781473
Yamamoto T, Yamashita H, Mukai K, Watanabe H, Kubota M, Chaen H, Fukuda S (2006b) Construction and characterization of chimeric enzymes of kojibiose phosphorylase and trehalose phosphorylase from Thermoanaerobacter brockii Carbohydr Res 341:2350–2359. https://doi.org/10.1016/j.carres.2006.06.024
doi: 10.1016/j.carres.2006.06.024
pubmed: 16872587
Yamamoto T, Nishio-Kosaka M, Izawa S, Aga H, Nishimoto T, Chaen H, Fukuda S (2011) Enzymatic properties of recombinant kojibiose phosphorylase from Caldicellulosiruptor saccharolyticus ATCC43494. Biosci Biotechnol Biochem 75:1208–1210. https://doi.org/10.1271/bbb.110116
Yang J, Hoffmeister D, Liu L, Fu X, Thorson JS (2004) Natural product glycorandomization. Bioorg Med Chem 12:1577–1584. https://doi.org/10.1016/j.bmc.2003.12.046
doi: 10.1016/j.bmc.2003.12.046
pubmed: 15112655
Yoshida M, Nakamura N, Horikoshi K (1998) Production of trehalose by a dual enzyme system of immobilized maltose phosphorylase and trehalose phosphorylase. Enzyme Microb Technol 22:71–75. https://doi.org/10.1016/S0141-0229(97)00132-4
doi: 10.1016/S0141-0229(97)00132-4
Zhang T, Yang J, Tian C, Ren C, Chen P, Men Y, Sun Y (2020) High-yield biosynthesis of glucosylglycerol through coupling phosphorolysis and transglycosylation reactions. J Agric Food Chem 68:15249–15256. https://doi.org/10.1021/acs.jafc.0c04851
doi: 10.1021/acs.jafc.0c04851
pubmed: 33306378
Zilli DMW, Lopes RG, Alves SL, Barros LM, Miletti LC, Stambuk BU (2015) Secretion of the acid trehalase encoded by the CgATH1 gene allows trehalose fermentation by Candida Glabrata Microbiol Res 179:12–19. https://doi.org/10.1016/j.micres.2015.06.008
doi: 10.1016/j.micres.2015.06.008
pubmed: 26411890