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Chitin-Active Lytic Polysaccharide Monooxygenases

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Book cover Targeting Chitin-containing Organisms

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 1142))

Abstract

Lytic polysaccharide monooxygenases (LPMOs) are copper-dependent enzymes that catalyze the cleavage of 1,4-glycosidic bonds various plant cell wall polysaccharides and chitin. In contrast to glycoside hydrolases, LPMOs are active on the crystalline regions of polysaccharides and thus synergize with hydrolytic enzymes. This synergism leads to an overall increase in the biomass-degradation activity of enzyme mixtures. Chitin-active LPMOs were discovered in 2010 and are currently classified in families AA10, AA11, and AA15 of the Carbohydrate-Active enZYmes database, which include LPMOs from bacteria, fungi, insects, and viruses. LPMOs have become important enzymes both industrially and scientifically and, in this chapter, we provide a brief introduction to chitin-active LPMOs including a summary of the 20+ chitin-active LPMOs that have been characterized so far. Then, we describe their structural features, catalytic mechanism, and appended carbohydrate modules. Finally, we show how chitin-active LPMOs can be used to perform chemo-enzymatic modification of chitin substrates.

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References

  • Aachmann FL et al (2012) NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions. Proc Natl Acad Sci USA 109(46):18779–18784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Agger JW et al (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci USA 111(17):6287–6292

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bacik J et al (2017) Neutron and atomic resolution X-ray structures of a lytic polysac- charide monooxygenase reveal copper-mediated dioxygen binding and evidence for N-terminal deprotonation. Biochemistry 56:2529–2532

    Article  CAS  PubMed  Google Scholar 

  • Beeson WT et al (2012) Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J Am Chem Soc 134(2):890–892

    Article  CAS  PubMed  Google Scholar 

  • Bennati-Granier C et al (2015) Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol Biofuels 8(90):90–103

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bissaro B et al (2018) How a lytic polysaccharide monooxygenase binds crystalline chitin. Biochemistry 57(12):1893–1906

    Article  CAS  PubMed  Google Scholar 

  • Bissaro B et al (2017) Oxidative cleavage of polysaccharides by monocopper enzymes depends on H2O2. Nat Chem Biol 13(10):1123–1128

    Article  CAS  PubMed  Google Scholar 

  • Boraston AB et al (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382:769–781

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borisova AS et al (2015) Structural and functional characterization of a lytic polysaccharide monooxygenase with broad substrate specificity. J Biol Chem 290(38):22955–22969

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Breslmayr E et al (2018) A fast and sensitive activity assay for lytic polysaccharide monooxygenase. Biotechnol Biofuels 11(1)

    Google Scholar 

  • Brun E et al (1997) Solution structure of the cellulose-binding domain of the endoglucanase Z secreted by Erwinia chrysanthemi. Biochemistry 36(51):16074–16086

    Article  CAS  PubMed  Google Scholar 

  • Chaplin AK et al (2016) Heterogeneity in the Histidine-brace Copper Coordination Sphere in Auxiliary Activity Family 10 (AA10) Lytic Polysaccharide Monooxygenases. J Biol Chem 291(24):12838–50

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chiu E et al (2015) Structural basis for the enhancement of virulence by viral spindles and their in vivo crystallization. Proc Natl Acad Sci 112(13):201418798

    Article  CAS  Google Scholar 

  • Courtade G et al (2015) 1H, 13C, 15N resonance assignment of the chitin-active lytic polysaccharide monooxygenase BlLPMO10A from Bacillus licheniformis. Biomol NMR Assign 9(1):207–210

    Article  CAS  PubMed  Google Scholar 

  • Courtade G et al (2018) The carbohydrate-binding module and linker of a modular lytic polysaccharide monooxygenase promote localized cellulose oxidation. J Biol Chem 293(34):13006–13015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couturier M et al (2018) Lytic xylan oxidases from wood-decay fungi unlock biomass degradation. Nat Chem Biol 14:306–310

    Article  CAS  PubMed  Google Scholar 

  • Crasson O et al (2017) Human chitotriosidase: catalytic domain or carbohydrate binding module, who’s leading HCHT’s biological function. Scientif Rep 7:2768–2777

    Article  CAS  Google Scholar 

  • Crouch LI et al (2016) The contribution of non-catalytic carbohydrate binding modules to the activity lytic polysaccharide monooxygenases. J Biol Chem 291(14):7439–7449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Eibinger M et al (2014) Cellulose surface degradation by a lytic polysaccharide monooxygenase and its effect on cellulase hydrolytic efficiency. J Biol Chem 289(52):35929–35938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fadel F et al (2016) X-Ray crystal structure of the full length human chitotriosidase (CHIT1) reveals features of its chitin binding domain. PLoS One 11(4):1–15

    Article  CAS  Google Scholar 

  • Forsberg Z et al (2011) Cleavage of cellulose by a CBM33 protein. Protein Sci Publ Protein Soc 20(9):1479–1483

    Article  CAS  Google Scholar 

  • Forsberg Z, Røhr AK et al (2014a) Comparative study of two chitin-active and two cellulose-active AA10-type lytic polysaccharide monooxygenases. Biochemistry 53(10):1647–1656

    Article  CAS  PubMed  Google Scholar 

  • Forsberg Z et al (2016) Structural and functional analysis of a lytic polysaccharide monooxygenase important for efficient utilization of chitin in Cellvibrio japonicus. J Biol Chem 291(14):7300–7312

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forsberg Z, Mackenzie AK et al (2014b) Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases. Proc Natl Acad Sci USA 111(23):8446–8451

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Forsberg Z et al (2018) Structural determinants of bacterial lytic polysaccharide monooxygenase functionality. J Biol Chem 293(4):1397–1412

    Article  CAS  PubMed  Google Scholar 

  • Frandsen KEH et al (2016) The molecular basis of polysaccharide cleavage by lytic polysaccharide monooxygenases. Nat Chem Biol 12:298–303

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frandsen KEH, Lo Leggio L (2016) Lytic polysaccharide monooxygenases: a crystallographer’s view on a new class of biomass-degrading enzymes. IUCrJ 3:448–467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frommhagen M et al (2015) Discovery of the combined oxidative cleavage of plant xylan and cellulose by a new fungal polysaccharide monooxygenase. Biotechnol Biofuels 8(101):101–113

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Frommhagen M et al (2016) Lytic polysaccharide monooxygenases from Myceliophthora thermophila C1 differ in substrate preference and reducing agent specificity. Biotechnol Biofuels 9(1):186

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gregory RC et al (2016) Activity, stability and 3-D structure of the Cu(II) form of a chitin-active lytic polysaccharide monooxygenase from Bacillus amyloliquefaciens. Dalton Trans 45:16904–16912

    Article  CAS  PubMed  Google Scholar 

  • Gudmundsson M et al (2014) Structural and electronic snapshots during the transition from a Cu(II) to Cu(I) metal center of a lytic polysaccharide monooxygenase by X-ray photoreduction. J Biol Chem 289(27):18782–92

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hangasky JA, Iavarone AT, Marletta MA (2018) Reactivity of O2 versus H2O2 with polysaccharide monooxygenases. Proc Nat Acad Sci

    Google Scholar 

  • Harris PV et al (2010) Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry 49(15):3305–3316

    Article  CAS  PubMed  Google Scholar 

  • Hemsworth GR et al (2014) Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat Chem Biol 10(2):122–126

    Article  CAS  PubMed  Google Scholar 

  • Hemsworth GR et al (2013) The copper active site of CBM33 polysaccharide oxygenases. J Am Chem Soc 135(16):6069–6077

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horn SJ et al (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5:45–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hudson KL et al (2015) Carbohydrate-aromatic interactions in proteins. J Am Chem Soc 137:15152–15160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hult E et al (2005) Molecular directionality in crystalline β-chitin: hydrolysis by chitinases A and B from Serratia marcescens 2170. Biochem J 388:851–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Igarashi K et al (2014) Two-way traffic of glycoside hydrolase family 18 processive chitinases on crystalline chitin. Nat Commun 5:1–7

    Article  CAS  Google Scholar 

  • Isaksen T et al (2014) A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J Biol Chem 289(5):2632–2642

    Article  CAS  PubMed  Google Scholar 

  • Kari J et al (2014) Kinetics of cellobiohydrolase (Cel7A) variants with lowered substrate affinity. J Biol Chem 289(47):32459–32468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Karkehabadi S et al (2008) The first structure of a glycoside hydrolase family 61 member, Cel61B from Hypocrea jecorina, at 1.6 Å resolution. J Mol Biol 383(1):144–154

    Google Scholar 

  • Kojima Y et al (2016) A lytic polysaccharide monooxygenase with broad xyloglucan specificity from the brown-rot fungus Gloeophyllum trabeum and its action on cellulose-xyloglucan complexes. Appl Environ Microbiol 82(22):6557–6572

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kracher D et al (2016) Extracellular electron transfer systems fuel cellulose oxidative degradation. Science (New York, N.Y.), 352(6289):1098–1101

    Google Scholar 

  • Kruer-Zerhusen N et al (2017) Structure of a Thermobifida fusca lytic polysaccharide monooxygenase and mutagenesis of key residues. Biotechnol Biofuels 10(1):1–12

    Article  CAS  Google Scholar 

  • Langston JA et al (2011) Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77(19):7007–7015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levasseur A et al (2013) Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol Biofuels 6:41–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loose JSM et al (2014) A rapid quantitative activity assay shows that the Vibrio cholerae colonization factor GbpA is an active lytic polysaccharide monooxygenase. FEBS Lett 588(18):3435–3440

    Article  CAS  PubMed  Google Scholar 

  • Loose JSM et al (2016) Activation of bacterial lytic polysaccharide monooxygenases with cellobiose dehydrogenase. Protein Sci

    Google Scholar 

  • Loose JSM et al (2018) Multipoint precision binding of substrate protects lytic polysaccharide monooxygenases from self-destructive off-pathway processes. Biochemistry 57(28):4114–4124

    Article  CAS  PubMed  Google Scholar 

  • Lo Leggio L et al (2015) Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase. Nat Commun 6:5961–5969

    Article  CAS  PubMed  Google Scholar 

  • McLean BW et al (2002) Carbohydrate-binding modules recognize fine substructures of cellulose. J Biol Chem 277(52):50245–50254

    Article  CAS  PubMed  Google Scholar 

  • Mekasha S et al (2016) Structural and functional characterization of a small chitin-active lytic polysaccharide monooxygenase domain of a multi-modular chitinase from Jonesia denitrificans S. Ferguson. FEBS Lett 590(1):34–42

    Google Scholar 

  • Monreal J, Reese ET (1969) The chitinase of Serratia marcescens. Can J Microbiol 15(7):689–696

    Article  CAS  PubMed  Google Scholar 

  • Moser F et al (2008) Regulation and characterization of Thermobifida fusca carbohydrate-binding module proteins E7 and E8. Biotechnol Bioeng 100(6):1066–1077

    Article  CAS  PubMed  Google Scholar 

  • Mutahir Z et al (2018) Characterization and synergistic action of a tetra-modular lytic polysaccharide monooxygenase from Bacillus cereus. FEBS Lett 592(15):2562–2571

    Article  CAS  PubMed  Google Scholar 

  • Nakagawa YS et al (2015) A small lytic polysaccharide monooxygenase from Streptomyces griseus targeting α-and β-chitin. FEBS J

    Google Scholar 

  • Paspaliari DK et al (2015) Listeria monocytogenes has a functional chitinolytic system and an active lytic polysaccharide monooxygenase. FEBS J 282(5):921–936

    Article  CAS  PubMed  Google Scholar 

  • Peisach J, Blumberg WE (1974) Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins. Arch Biochem Biophys 165(2):691–708

    Article  CAS  PubMed  Google Scholar 

  • Petrović DM et al (2018) Methylation of the N-terminal histidine protects a lytic polysaccharide monooxygenase from auto-oxidative inactivation. Protein Sci 27:1635–1650

    Article  CAS  Google Scholar 

  • Phillips CM et al (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 6(12):1399–1406

    Article  CAS  PubMed  Google Scholar 

  • Quinlan RJ et al (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci USA 108(37):15079–15084

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabbadin F et al (2018) An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion. Nat Commun 9(756):756–767

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tan T-C et al (2015) Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation. Nat Commun 6(May):7542–7552

    Article  PubMed  Google Scholar 

  • Vaaje-Kolstad G et al (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science (New York, NY), 330(6001):219–222

    Google Scholar 

  • Vaaje-Kolstad G et al (2012) Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J Mol Biol 416(2):239–254

    Article  CAS  PubMed  Google Scholar 

  • Vaaje-Kolstad G, Houston DR et al (2005a) Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J Biol Chem 280(12):11313–11319

    Article  CAS  PubMed  Google Scholar 

  • Vaaje-Kolstad G et al (2013) The chitinolytic machinery of Serratia marcescens-a model system for enzymatic degradation of recalcitrant polysaccharides. FEBS J 280(13):3028–3049

    Article  CAS  PubMed  Google Scholar 

  • Vaaje-Kolstad G, Horn SJ et al (2005b) The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 280(31):28492–28497

    Article  CAS  PubMed  Google Scholar 

  • Valenzuela SV et al (2017) Fast purification method of functional LPMOs from Streptomyces ambofaciens by affinity adsorption. Carbohyd Res 448:205–211

    Article  CAS  Google Scholar 

  • Vermaas JV et al (2015) Effects of lytic polysaccharide monooxygenase oxidation on cellulose structure and binding of oxidized cellulose oligomers to cellulases. J Phys Chem B 119(20):6129–6143

    Article  CAS  PubMed  Google Scholar 

  • Vu VV et al (2014) A family of starch-active polysaccharide monooxygenases. Proc Natl Acad Sci USA 111(38):13822–13827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vuong TV et al (2017) Microplate-based detection of lytic polysaccharide monooxygenase activity by fluorescence-labeling of insoluble oxidized products. Biomacromol 18(2):610–616

    Article  CAS  Google Scholar 

  • Walton PH, Davies GJ (2016) On the catalytic mechanisms of lytic polysaccharide monooxygenases. Curr Opin Chem Biol 31:195–207

    Article  CAS  PubMed  Google Scholar 

  • Wang D, Li J, Wong ACY et al (2018a) A colorimetric assay to rapidly determine the activities of lytic polysaccharide monooxygenases. Biotechnol Biofuels 11(1):1–11

    Article  CAS  Google Scholar 

  • Wang D, Li J, Salazar-Alvarez G et al (2018b) Production of functionalised chitins assisted by fungal lytic polysaccharide monooxygenase. Green Chem 20(9):2091–2100

    Article  CAS  Google Scholar 

  • Westereng B et al (2015) Enzymatic cellulose oxidation is linked to lignin by long-range electron transfer. Scientif Rep 5:18561–18577

    Article  CAS  Google Scholar 

  • Wong E et al (2012) The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces. PLoS Pathog 8(1):1–12

    Article  CAS  Google Scholar 

  • Xu GY et al (1995) Solution structure of a cellulose-binding domain from Cellulomonas fimi by nuclear magnetic resonance spectroscopy. Biochemistry 34(21):6993–7009

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Finn L. Aachmann .

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Courtade, G., Aachmann, F.L. (2019). Chitin-Active Lytic Polysaccharide Monooxygenases. In: Yang, Q., Fukamizo, T. (eds) Targeting Chitin-containing Organisms. Advances in Experimental Medicine and Biology, vol 1142. Springer, Singapore. https://doi.org/10.1007/978-981-13-7318-3_6

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