Polysaccharide Monooxygenase-catalyzed Oxidation of Cellulose to Glucuronic Acid-containing Cello-oligosaccharides

Overview

Journal Biotechnol Biofuels

Publisher Biomed Central

Specialty Biotechnology

Date 2019 Mar 13

PMID 30858879

Citations 8

Authors

Jinyin Chen

Xiuna Guo

Min Zhu

Chen Chen

Duochuan Li

Affiliations

Soon will be listed here.

Abstract

Background: Polysaccharide monooxygenases (PMOs) play an important role in the enzymatic degradation of cellulose. They have been demonstrated to able to C6-oxidize cellulose to produce C6-hexodialdoses. However, the biological function of C6 oxidation of PMOs remains unknown. In particular, it is unclear whether C6-hexodialdoses can be further oxidized to uronic acid (glucuronic acid-containing oligosaccharides).

Results: A PMO gene, , was isolated from and expressed in . This PMO (HiPMO1), belonging to the auxiliary activity 9 (AA9) family, was shown to able to cleave cellulose to yield non-oxidized and oxidized cello-oligosaccharides. The enzyme oxidizes C6 positions in cellulose to form glucuronic acid-containing cello-oligosaccharides, followed by hydrolysis with beta-glucosidase and beta-glucuronidase to yield glucose, glucuronic acid, and saccharic acid. This indicates that HiPMO1 can catalyze C6 oxidation of hydroxyl groups of cellulose to carboxylic groups.

Conclusions: HiPMO1 oxidizes C6 of cellulose to form glucuronic acid-containing cello-oligosaccharides followed by hydrolysis with beta-glucosidase and beta-glucuronidase to yield glucose, glucuronic acid, and saccharic acid, and even possibly by beta-eliminative cleavage to produce unsaturated cello-oligosaccharides. This study provides a new mechanism for cellulose cleavage by C6 oxidation of HiPMO1.

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References

Whittaker M, Kersten P, Cullen D, Whittaker J . Identification of catalytic residues in glyoxal oxidase by targeted mutagenesis. J Biol Chem. 1999; 274(51):36226-32. DOI: 10.1074/jbc.274.51.36226. View

Dell A, Morris H . Glycoprotein structure determination by mass spectrometry. Science. 2001; 291(5512):2351-6. DOI: 10.1126/science.1058890. View

Whittaker J . Free radical catalysis by galactose oxidase. Chem Rev. 2003; 103(6):2347-63. DOI: 10.1021/cr020425z. View

LOWRY O, ROSEBROUGH N, FARR A, RANDALL R . Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. View

Shinohara Y, Furukawa J, Niikura K, Miura N, Nishimura S . Direct N-glycan profiling in the presence of tryptic peptides on MALDI-TOF by controlled ion enhancement and suppression upon glycan-selective derivatization. Anal Chem. 2004; 76(23):6989-97. DOI: 10.1021/ac0492766. View

Linster C, Van Schaftingen E . Glucuronate, the precursor of vitamin C, is directly formed from UDP-glucuronate in liver. FEBS J. 2006; 273(7):1516-27. DOI: 10.1111/j.1742-4658.2006.05172.x. View

Zhang Y, Himmel M, Mielenz J . Outlook for cellulase improvement: screening and selection strategies. Biotechnol Adv. 2006; 24(5):452-81. DOI: 10.1016/j.biotechadv.2006.03.003. View

Kersten P, Cullen D . Extracellular oxidative systems of the lignin-degrading Basidiomycete Phanerochaete chrysosporium. Fungal Genet Biol. 2006; 44(2):77-87. DOI: 10.1016/j.fgb.2006.07.007. View

Himmel M, Ding S, Johnson D, Adney W, Nimlos M, Brady J . Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science. 2007; 315(5813):804-7. DOI: 10.1126/science.1137016. View

10.

Karkehabadi S, Hansson H, Kim S, Piens K, Mitchinson C, Sandgren M . The first structure of a glycoside hydrolase family 61 member, Cel61B from Hypocrea jecorina, at 1.6 A resolution. J Mol Biol. 2008; 383(1):144-54. DOI: 10.1016/j.jmb.2008.08.016. View

11.

Zoltaszek R, Hanausek M, Kilianska Z, Walaszek Z . [The biological role of D-glucaric acid and its derivatives: potential use in medicine]. Postepy Hig Med Dosw (Online). 2008; 62:451-62. View

12.

Carroll A, Somerville C . Cellulosic biofuels. Annu Rev Plant Biol. 2008; 60:165-82. DOI: 10.1146/annurev.arplant.043008.092125. View

13.

Moon T, Yoon S, Lanza A, Roy-Mayhew J, Jones Prather K . Production of glucaric acid from a synthetic pathway in recombinant Escherichia coli. Appl Environ Microbiol. 2008; 75(3):589-95. PMC: 2632142. DOI: 10.1128/AEM.00973-08. View

14.

Parikka K, Tenkanen M . Oxidation of methyl alpha-D-galactopyranoside by galactose oxidase: products formed and optimization of reaction conditions for production of aldehyde. Carbohydr Res. 2008; 344(1):14-20. DOI: 10.1016/j.carres.2008.08.020. View

15.

Konno N, Ishida T, Igarashi K, Fushinobu S, Habu N, Samejima M . Crystal structure of polysaccharide lyase family 20 endo-beta-1,4-glucuronan lyase from the filamentous fungus Trichoderma reesei. FEBS Lett. 2009; 583(8):1323-6. DOI: 10.1016/j.febslet.2009.03.034. View

16.

Wisniewski J, Zougman A, Nagaraj N, Mann M . Universal sample preparation method for proteome analysis. Nat Methods. 2009; 6(5):359-62. DOI: 10.1038/nmeth.1322. View

17.

Wilson D . Cellulases and biofuels. Curr Opin Biotechnol. 2009; 20(3):295-9. DOI: 10.1016/j.copbio.2009.05.007. View

18.

Li A, Yu K, Liu H, Zhang J, Li H, Li D . Two novel thermostable chitinase genes from thermophilic fungi: cloning, expression and characterization. Bioresour Technol. 2010; 101(14):5546-51. DOI: 10.1016/j.biortech.2010.02.058. View

19.

Harris P, Welner D, McFarland K, Re E, Poulsen J, Brown K . Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry. 2010; 49(15):3305-16. DOI: 10.1021/bi100009p. View

20.

Service R . Is there a road ahead for cellulosic ethanol?. Science. 2010; 329(5993):784-5. DOI: 10.1126/science.329.5993.784. View