Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Garajova, Sona ^a,b   Mathieu, Yann ^a   Beccia, Maria Rosa ^c   Bennati Granier, Chloé ^a   Biaso, Frédéric ^c   Fanuel, Mathieu ^d   Ropartz, David ^d   Guigliarelli, Bruno ^c   Record, Eric ^a   Rogniaux, Hélène ^d   Henrissat, Bernard ^e,f   Berrin, Jean Guy ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d INRA   (France)

^e Centre National de la Recherche Scientifique   (France)

^f KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CELLOBIOSE-QUINONE OXIDOREDUCTASE; FLAVOPROTEIN; FUNGAL PROTEIN; MIXED FUNCTION OXIDASE; OXIDOREDUCTASE;

CHEMISTRY; ENZYMOLOGY; GENETICS; PODOSPORA; PROTEIN DOMAIN;

CARBOHYDRATE DEHYDROGENASES; FLAVOPROTEINS; FUNGAL PROTEINS; MIXED FUNCTION OXYGENASES; PODOSPORA; PROTEIN DOMAINS;

EID: 84975502151     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep28276     Document Type: Article

References (47)

1. Harris, P. V. et al. Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: Structure and function of a large, enigmatic family. Biochemistry 49, 3305-3316 (2010).
2. Vaaje-Kolstad, G. et al. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharide. Science 330, 219-222 (2010).
3. Johansen, K. S. Discovery and industrial applications of lytic polysaccharide mono-oxygenases. Biochem. Soc. Trans. 44, 143-149 (2016).
4. Lombard, V., Golaconda Ramulu, H., Drula, E., Coutinho, P. M. & Henrissat, B. The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42, 490-495 (2014).
5. Quinlan, R. J. et al. Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc. Natl. Acad. Sci. USA 108, 15079-84 (2011).
6. Levasseur, A., Drula, E., Lombard, V., Coutinho, P. M. & Henrissat, B. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol. Biofuels 6, 41 (2013).
7. Espagne, E. et al. The genome sequence of the model ascomycete fungus Podospora anserina. Genome Biol. 9, R77 (2008).
8. Bey, M. et al. Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (Family GH61) from Podospora anserina. Appl. Environ. Microbiol. 79, 488-496 (2013).
9. Bennati-Granier, C. et al. Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol. Biofuels 8, 90 (2015).
10. Forsberg, Z. et al. Cleavage of cellulose by a CBM33 protein. Protein Sci. 20, 1479-1483 (2011).
11. Lo Leggio, L. et al. Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase. Nat. Commun. 6, 5961 (2015).
12. Westereng, B. et al. Enzymatic cellulose oxidation is linked to lignin by long-range electron transfer. Sci. Rep. 5, 18561 (2015).
13. Navarro, D. et al. Fast solubilization of recalcitrant cellulosic biomass by the basidiomycete fungus Laetisaria arvalis involves successive secretion of oxidative and hydrolytic enzymes. Biotechnol. Biofuels 7, 143 (2014).
14. Levasseur, A. et al. The genome of the white-rot fungus Pycnoporus cinnabarinus: a basidiomycete model with a versatile arsenal for lignocellulosic biomass breakdown. BMC Genomics 15, 486 (2014).
15. Couturier, M. et al. Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus. Biotechnol. Biofuels 8, 216 (2015).
16. Poidevin, L. et al. Comparative analyses of Podospora anserina secretomes reveal a large array of lignocellulose-active enzymes. Appl. Microbiol. Biotechnol. 98, 7457-7469 (2014).
17. Kracher, D. et al. Fungal secretomes enhance sugar beet pulp hydrolysis. Biotechnol. J. 9, 483-492 (2014).
18. Henriksson, G., Johansson, G. & Pettersson, G. A critical review of cellobiose dehydrogenases. J. Biotechnol. 78, 93-113 (2000).
19. Cameron, M. D. & Aust, S. D. Cellobiose dehydrogenase-an extracellular fungal flavocytochrome. Enzyme Microb. Technol. 28, 129-138 (2001).
20. Zamocky, M. et al. Cellobiose dehydrogenase - a flavocytochrome from wood-degrading, phytopathogenic and saprotropic fungi. Curr. Protein Pept. Sci. 7, 255-280 (2006).
21. Langston, J. a. et al. Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl. Environ. Microbiol. 77, 7007-7015 (2011).
22. Phillips, C. M., Beeson, W. T., Cate, J. H. & Marletta, M. Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem. Biol. 6, 1399-406 (2011).
23. Sygmund, C. et al. Characterization of the two Neurospora crassa cellobiose dehydrogenases and their connection to oxidative cellulose degradation. Appl. Environ. Microbiol. 78, 6161-6171 (2012).
24. Beeson, W. T., Phillips, C. M., Cate, J. H. D. & Marletta, M. a. Oxidative cleavage of cellulose by fungal copper-dependent polysaccharide monooxygenases. J. Am. Chem. Soc. 134, 890-892 (2012).
25. Tan, T.-C. et al. Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation. Nat. Commun. 6, 7542 (2015).
26. Couturier, M. et al. Post-genomic analyses of fungal lignocellulosic biomass degradation reveal the unexpected potential of the plant pathogen Ustilago maydis. BMC Genomics 13, 57 (2012).
27. Mathieu, Y. et al. Secreted aryl alcohol quinone oxidoreductases from Pycnoporus cinnabarinus provides new activities and insights into fungal degradation of plant biomass. Appl. Environ. Microbiol. 82, 2411-2423 (2016).
28. Couturier, M. et al. Characterization of a new aryl-alcohol oxidase secreted by the phytopathogenic fungus Ustilago maydis. Appl. Microbiol. Biotechnol. 100, 697-706 (2016).
29. Piumi, F. et al. A novel glucose dehydrogenase from the white-rot fungus Pycnoporus cinnabarinus: production in Aspergillus niger and physicochemical characterization of the recombinant enzyme. Appl. Microbiol. Biotechnol. 98, 10105-10118 (2014).
30. Isaksen, T. et al. A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J. Biol. Chem. 289, 2632-2642 (2014).
31. Borisova, A. S. et al. Structural and functional characterization of a lytic polysaccharide monooxygenase with broad substrate specificity. J. Biol. Chem. jbc.M115.660183 (2015).
32. Peisach, J. & Blumberg, W. E. Structural implications derived from the analysis of electron paramagnetic resonance spectra of natural and artificial copper proteins. Arch. Biochem. Biophys. 165, 691-708 (1974).
33. Henriksson, G., Sild, V., Szabó, I. J., Pettersson, G. & Johansson, G. Substrate specificity of cellobiose dehydrogenase from Phanerochaete chrysosporium. Biochim. Biophys. Acta-Protein Struct. Mol. Enzymol. 1383, 48-54 (1998).
34. Mason, M. G., Wilson, M. T., Ball, A. & Nicholls, P. Oxygen reduction by cellobiose oxidoreductase: The role of the haem group. FEBS Lett. 518, 29-32 (2002).
35. Tedeshi, G., Chen, S. & Massey, V. DT-diaphorase redox potential, steady-state, and rapid reaction studies. J. Biol. Chem. 270, 1198-1204 (1995).
36. Chobot, V., Hadacek, F., Weckwerth, W. & Kubicova, L. Iron chelation and redox chemistry of anthranilic acid and 3-hydroxyanthranilic acid: A comparison of two structurally related kynurenine pathway metabolites to obtain improved insights into their potential role in neurological disease development. J. Organomet. Chem. 782, 103-110 (2015).
37. Fabbrini, M., Galli, C. & Gentili, P. Comparing the catalytic efficiency of some mediators of laccase. J. Mol. Catal.-B Enzym. 16, 231-240 (2002).
38. Cannella, D. et al. Light-driven oxidation of polysaccharides by photosynthetic pigments and a metalloenzyme. Nat. Commun. 7, 11134 (2016).
39. Kracher, D. et al. Extracellular electron transfer systems fuel cellulose oxidative degradation. Science (2016) in press.
40. Wood, T. M. Preparation of crystalline, amorphous, and dyed cellulase substrates. Methods Enzymol. 160, 19-25 (1988).
41. Westereng, B. et al. Efficient separation of oxidized cello-oligosaccharides generated by cellulose degrading lytic polysaccharide monooxygenases. J. Chromatogr. A. 1271, 144-152 (2013).
42. Hemsworth, G. R., Davies, G. J. & Walton, P. H. Recent insights into copper-containing lytic polysaccharide mono-oxygenases. Curr. Opin. Struct. Biol. 23, 660-668 (2013).
43. Forsberg, Z. et al. Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases. Proc. Natl. Acad. Sci. USA 111, 8446-51 (2014).
44. Aachmann, F. L., Sørlie, M., Skjåk-Bræk, G., Eijsink, V. G. H. & Vaaje-Kolstad, G. NMR structure of a lytic polysaccharide monooxygenase provides insight into copper binding, protein dynamics, and substrate interactions. Proc. Natl. Acad. Sci. USA 109, 18779-18784 (2012).
45. Hemsworth, G. R., Henrissat, B., Davies, G. J. & Walton, P. H. Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat. Chem. Biol. 10, 122-6 (2014).
46. Schulz, C., Kittl, R., Ludwig, R. & Gorton, L. Direct Electron Transfer from the FAD Cofactor of Cellobiose Dehydrogenase to Electrodes. ASC Catal. 6, 555-563 (2016).
47. Igarashi, K. et al. Cellobiose Dehydrogenase from the Fungi Phanerochaete chrysosporium and Humicola. J. Biol. Chem. 274, 3338-3344 (1999).