Current understanding of substrate specificity and regioselectivity of LPMOs

Xiaoli Zhou , Honghui Zhu

Bioresources and Bioprocessing ›› 2020, Vol. 7 ›› Issue (1) : 11

PDF
Bioresources and Bioprocessing ›› 2020, Vol. 7 ›› Issue (1) : 11 DOI: 10.1186/s40643-020-0300-6
Review

Current understanding of substrate specificity and regioselectivity of LPMOs

Author information +
History +
PDF

Abstract

Renewable biomass such as cellulose and chitin are the most abundant sustainable sources of energy and materials. However, due to the low degradation efficiency of these recalcitrant substrates by conventional hydrolases, these biomass resources cannot be utilized efficiently. In 2010, the discovery of lytic polysaccharide monooxygenases (LPMOs) led to a major breakthrough. Currently, LPMOs are distributed in 7 families in CAZy database, including AA9–11 and AA13–16, with different species origins, substrate specificity and oxidative regioselectivity. Effective application of LPMOs in the biotransformation of biomass resources needs the elucidation of the molecular basis of their function. Since the discovery of LPMOs, great advances have been made in the study of their substrate specificity and regioselectivity, as well as their structural basis, which will be reviewed below.

Keywords

Lytic polysaccharide monooxygenase / LPMO / Substrate specificity / Regioselectivity

Cite this article

Download citation ▾
Xiaoli Zhou, Honghui Zhu. Current understanding of substrate specificity and regioselectivity of LPMOs. Bioresources and Bioprocessing, 2020, 7(1): 11 DOI:10.1186/s40643-020-0300-6

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Aachmann FL, Sorlie M, Skjak-Braek G, Eijsink VG, 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, 2012, 109: 18779-18784.

[2]

Agger JW, Isaksen T, Varnai A, Vidal-Melgosa S, Willats WG, Ludwig R, Horn SJ, Eijsink VG, Westereng B. Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci USA, 2014, 111: 6287-6292.

[3]

Bacik JP, Mekasha S, Forsberg Z, Kovalevsky AY, Vaaje-Kolstad G, Eijsink VGH, Nix JC, Coates L, Cuneo MJ, Unkefer CJ, Chen JC. Neutron and atomic resolution X-ray structures of a lytic polysaccharide monooxygenase reveal copper-mediated dioxygen binding and evidence for N-terminal deprotonation. Biochemistry, 2017, 56: 2529-2532.

[4]

Beeson WT, Vu VV, Span EA, Phillips CM, Marletta MA. Cellulose degradation by polysaccharide monooxygenases. Annu Rev Biochem, 2015, 84: 923-946.

[5]

Bennati-Granier C, Garajova S, Champion C, Grisel S, Haon M, Zhou S, Fanuel M, Ropartz D, Rogniaux H, Gimbert I, Record E, Berrin JG. Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol Biofuels, 2015, 8: 90.

[6]

Bey M, Zhou S, Poidevin L, Henrissat B, Coutinho PM, Berrin JG, Sigoillot JC. Cello-oligosaccharide oxidation reveals differences between two lytic polysaccharide monooxygenases (family GH61) from Podospora anserina. Appl Environ Microbiol, 2013, 79: 488-496.

[7]

Bissaro B, Rohr AK, Muller G, Chylenski P, Skaugen M, Forsberg Z, Horn SJ, Vaaje-Kolstad G, Eijsink VGH. Oxidative cleavage of polysaccharides by monocopper enzymes depends on H2O2. Nat Chem Biol, 2017, 13: 1123-1128.

[8]

Bissaro B, Isaksen I, Vaaje-Kolstad G, Eijsink VGH, Rohr AK. How a lytic polysaccharide monooxygenase binds crystalline chitin. Biochemistry, 2018, 57: 1893-1906.

[9]

Book AJ, Yennamalli RM, Takasuka TE, Currie CR, Phillips GN Jr, Fox BG. Evolution of substrate specificity in bacterial AA10 lytic polysaccharide monooxygenases. Biotechnol Biofuels, 2014, 7: 109.

[10]

Borisova AS, Isaksen T, Dimarogona M, Kognole AA, Mathiesen G, Varnai A, Rohr AK, Payne CM, Sorlie M, Sandgren M, Eijsink VG. Structural and functional characterization of a lytic polysaccharide monooxygenase with broad substrate specificity. J Biol Chem, 2015, 290: 22955-22969.

[11]

Cannella D, Mollers KB, Frigaard NU, Jensen PE, Bjerrum MJ, Johansen KS, Felby C. Light-driven oxidation of polysaccharides by photosynthetic pigments and a metalloenzyme. Nat Commun, 2016, 7: 11134.

[12]

Chabbert B, Habrant A, Herbaut M, Foulon L, Aguie-Beghin V, Garajova S, Grisel S, Bennati-Granier C, Gimbert-Herpoel I, Jamme F, Refregiers M, Sandt C, Berrin JG, Paes G. Action of lytic polysaccharide monooxygenase on plant tissue is governed by cellular type. Sci Rep, 2017, 7: 17792.

[13]

Chalak A, Villares A, Moreau C, Haon M, Grisel S, d’Orlando A, Herpoel-Gimbert I, Labourel A, Cathala B, Berrin JG. Influence of the carbohydrate-binding module on the activity of a fungal AA9 lytic polysaccharide monooxygenase on cellulosic substrates. Biotechnol Biofuels, 2019, 12: 206.

[14]

Chaplin AK, Wilson MT, Hough MA, Svistunenko DA, Hemsworth GR, Walton PH, Vijgenboom E, Worrall JA. Heterogeneity in the histidine-brace copper coordination sphere in auxiliary activity family 10 (AA10) lytic polysaccharide monooxygenases. J Biol Chem, 2016, 291: 12838-12850.

[15]

Chen C, Chen J, Geng Z, Wang M, Liu N, Li D. Regioselectivity of oxidation by a polysaccharide monooxygenase from Chaetomium thermophilum. Biotechnol Biofuels, 2018, 11: 155.

[16]

Chiu E, Hijnen M, Bunker RD, Boudes M, Rajendran C, Aizel K, Olieric V, Schulze-Briese C, Mitsuhashi W, Young V, Ward VK, Bergoin M, Metcalf P, Coulibaly F. Structural basis for the enhancement of virulence by viral spindles and their in vivo crystallization. Proc Natl Acad Sci USA, 2015, 112: 3973-3978.

[17]

Correa TLR, Junior AT, Wolf LD, Buckeridge MS, Dos Santos LV, Murakami MT. An actinobacteria lytic polysaccharide monooxygenase acts on both cellulose and xylan to boost biomass saccharification. Biotechnol Biofuels, 2019, 12: 117.

[18]

Courtade G, Balzer S, Forsberg Z, Vaaje-Kolstad G, Eijsink VG, Aachmann FL. (1)H, (13)C, (15)N resonance assignment of the chitin-active lytic polysaccharide monooxygenase BlLPMO10A from Bacillus licheniformis. Biomol NMR Assign, 2015, 9: 207-210.

[19]

Courtade G, Wimmer R, Rohr AK, Preims M, Felice AK, Dimarogona M, Vaaje-Kolstad G, Sorlie M, Sandgren M, Ludwig R, Eijsink VG, Aachmann FL. Interactions of a fungal lytic polysaccharide monooxygenase with beta-glucan substrates and cellobiose dehydrogenase. Proc Natl Acad Sci USA, 2016, 113: 5922-5927.

[20]

Courtade G, Forsberg Z, Heggset EB, Eijsink VGH, Aachmann FL. The carbohydrate-binding module and linker of a modular lytic polysaccharide monooxygenase promote localized cellulose oxidation. J Biol Chem, 2018, 293: 13006-13015.

[21]

Couturier M, Ladeveze S, Sulzenbacher G, Ciano L, Fanuel M, Moreau C, Villares A, Cathala B, Chaspoul F, Frandsen KE, Labourel A, Herpoel-Gimbert I, Grisel S, Haon M, Lenfant N, Rogniaux H, Ropartz D, Davies GJ, Rosso MN, Walton PH, Henrissat B, Berrin JG. Lytic xylan oxidases from wood-decay fungi unlock biomass degradation. Nat Chem Biol, 2018, 14: 306-310.

[22]

Crouch LI, Labourel A, Walton PH, Davies GJ, Gilbert HJ. The contribution of non-catalytic carbohydrate binding modules to the activity of lytic polysaccharide monooxygenases. J Biol Chem, 2016, 291: 7439-7449.

[23]

Danneels B, Tanghe M, Joosten HJ, Gundinger T, Spadiut O, Stals I, Desmet T. A quantitative indicator diagram for lytic polysaccharide monooxygenases reveals the role of aromatic surface residues in HjLPMO9A regioselectivity. PLoS ONE, 2017, 12: e0178446.

[24]

Danneels B, Tanghe M, Desmet T. Structural features on the substrate-binding surface of fungal lytic polysaccharide monooxygenases determine their oxidative regioselectivity. Biotechnol J, 2019, 14: e1800211.

[25]

de Gouvea PF, Gerolamo LE, Bernardi AV, Pereira LMS, Uyemura SA, Dinamarco TM. Lytic Polysaccharide Monooxygenase from Aspergillus fumigatus can improve enzymatic cocktail activity during sugarcane bagasse hydrolysis. Protein Pept Lett, 2019, 26: 377-385.

[26]

Dimarogona M, Topakas E, Christakopoulos P. Recalcitrant polysaccharide degradation by novel oxidative biocatalysts. Appl Microbiol Biotechnol, 2013, 97: 8455-8465.

[27]

Eriksson KE, Pettersson B, Westermark U. Oxidation: an important enzyme reaction in fungal degradation of cellulose. FEBS Lett, 1974, 49: 282-285.

[28]

Fanuel M, Garajova S, Ropartz D, McGregor N, Brumer H, Rogniaux H, Berrin JG. The Podospora anserina lytic polysaccharide monooxygenase PaLPMO9H catalyzes oxidative cleavage of diverse plant cell wall matrix glycans. Biotechnol Biofuels, 2017, 10: 63.

[29]

Filiatrault-Chastel C, Navarro D, Haon M, Grisel S, Herpoel-Gimbert I, Chevret D, Fanuel M, Henrissat B, Heiss-Blanquet S, Margeot A, Berrin JG. AA16, a new lytic polysaccharide monooxygenase family identified in fungal secretomes. Biotechnol Biofuels, 2019, 12: 55.

[30]

Forsberg Z, Vaaje-Kolstad G, Westereng B, Bunaes AC, Stenstrom Y, MacKenzie A, Sorlie M, Horn SJ, Eijsink VG. Cleavage of cellulose by a CBM33 protein. Protein Sci, 2011, 20: 1479-1483.

[31]

Forsberg Z, Mackenzie AK, Sorlie M, Rohr AK, Helland R, Arvai AS, Vaaje-Kolstad G, Eijsink VG. Structural and functional characterization of a conserved pair of bacterial cellulose-oxidizing lytic polysaccharide monooxygenases. Proc Natl Acad Sci USA, 2014, 111: 8446-8451.

[32]

Forsberg Z, Rohr AK, Mekasha S, Andersson KK, Eijsink VG, Vaaje-Kolstad G, Sorlie M. Comparative study of two chitin-active and two cellulose-active AA10-type lytic polysaccharide monooxygenases. Biochemistry, 2014, 53: 1647-1656.

[33]

Forsberg Z, Nelson CE, Dalhus B, Mekasha S, Loose JS, Crouch LI, Rohr AK, Gardner JG, Eijsink VG, Vaaje-Kolstad G. Structural and functional analysis of a lytic polysaccharide monooxygenase important for efficient utilization of chitin in Cellvibrio japonicus. J Biol Chem, 2016, 291: 7300-7312.

[34]

Forsberg Z, Bissaro B, Gullesen J, Dalhus B, Vaaje-Kolstad G, Eijsink VGH. Structural determinants of bacterial lytic polysaccharide monooxygenase functionality. J Biol Chem, 2018, 293: 1397-1412.

[35]

Forsberg Z, Sørlie M, Petrović D, Courtade G, Aachmann FL, Vaaje-Kolstad G, Bissaro B, Røhr ÅK, Eijsink VG. Polysaccharide degradation by lytic polysaccharide monooxygenases. Curr Opin Struct Biol, 2019, 1(59): 54-64.

[36]

Fowler CA, Sabbadin F, Ciano L, Hemsworth GR, Elias L, Bruce N, McQueen-Mason S, Davies GJ, Walton PH. Discovery, activity and characterisation of an AA10 lytic polysaccharide oxygenase from the shipworm symbiont Teredinibacter turnerae. Biotechnol Biofuels, 2019, 12: 232.

[37]

Frandsen KE, Simmons TJ, Dupree P, Poulsen JC, Hemsworth GR, Ciano L, Johnston EM, Tovborg M, Johansen KS, von Freiesleben P, Marmuse L, Fort S, Cottaz S, Driguez H, Henrissat B, Lenfant N, Tuna F, Baldansuren A, Davies GJ, Lo Leggio L, Walton PH. The molecular basis of polysaccharide cleavage by lytic polysaccharide monooxygenases. Nat Chem Biol, 2016, 12: 298-303.

[38]

Frandsen KE, Poulsen JC, Tovborg M, Johansen KS, Lo Leggio L. Learning from oligosaccharide soaks of crystals of an AA13 lytic polysaccharide monooxygenase: crystal packing, ligand binding and active-site disorder. Acta Crystallogr D Struct Biol, 2017, 73: 64-76.

[39]

Frommhagen M, Sforza S, Westphal AH, Visser J, Hinz SW, Koetsier MJ, van Berkel WJ, Gruppen H, Kabel MA. Discovery of the combined oxidative cleavage of plant xylan and cellulose by a new fungal polysaccharide monooxygenase. Biotechnol Biofuels, 2015, 8: 101.

[40]

Frommhagen M, Koetsier MJ, Westphal AH, Visser J, Hinz SW, Vincken JP, van Berkel WJ, Kabel MA, Gruppen H. Lytic polysaccharide monooxygenases from Myceliophthora thermophila C1 differ in substrate preference and reducing agent specificity. Biotechnol Biofuels, 2016, 9: 186.

[41]

Frommhagen M, Mutte SK, Westphal AH, Koetsier MJ, Hinz SWA, Visser J, Vincken JP, Weijers D, van Berkel WJH, Gruppen H, Kabel MA. Boosting LPMO-driven lignocellulose degradation by polyphenol oxidase-activated lignin building blocks. Biotechnol Biofuels, 2017, 10: 121.

[42]

Frommhagen M, van Erven G, Sanders M, van Berkel WJH, Kabel MA, Gruppen H. RP-UHPLC-UV-ESI-MS/MS analysis of LPMO generated C4-oxidized gluco-oligosaccharides after non-reductive labeling with 2-aminobenzamide. Carbohydr Res, 2017, 448: 191-199.

[43]

Frommhagen M, Westphal AH, Hilgers R, Koetsier MJ, Hinz SWA, Visser J, Gruppen H, van Berkel WJH, Kabel MA. Quantification of the catalytic performance of C1-cellulose-specific lytic polysaccharide monooxygenases. Appl Microbiol Biotechnol, 2018, 102: 1281-1295.

[44]

Garajova S, Mathieu Y, Beccia MR, Bennati-Granier C, Biaso F, Fanuel M, Ropartz D, Guigliarelli B, Record E, Rogniaux H, Henrissat B, Berrin JG. Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose. Sci Rep, 2016, 6: 28276.

[45]

Gardner JG, Crouch L, Labourel A, Forsberg Z, Bukhman YV, Vaaje-Kolstad G, Gilbert HJ, Keating DH. Systems biology defines the biological significance of redox-active proteins during cellulose degradation in an aerobic bacterium. Mol Microbiol, 2014, 94(5): 1121-1133.

[46]

Ghatge SS, Telke AA, Waghmode TR, Lee Y, Lee KW, Oh DB, Shin HD, Kim SW. Multifunctional cellulolytic auxiliary activity protein HcAA10-2 from Hahella chejuensis enhances enzymatic hydrolysis of crystalline cellulose. Appl Microbiol Biotechnol, 2015, 99: 3041-3055.

[47]

Gregory RC, Hemsworth GR, Turkenburg JP, Hart SJ, Walton PH, Davies GJ. Activity, stability and 3-D structure of the Cu(ii) form of a chitin-active lytic polysaccharide monooxygenase from Bacillus amyloliquefaciens. Dalton Trans, 2016, 45: 16904-16912.

[48]

Gudmundsson M, Kim S, Wu M, Ishida T, Momeni MH, Vaaje-Kolstad G, Lundberg D, Royant A, Stahlberg J, Eijsink VG, Beckham GT, Sandgren M. 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, 2014, 289: 18782-18792.

[49]

Gusakov AV, Bulakhov AG, Demin IN, Sinitsyn AP. Monitoring of reactions catalyzed by lytic polysaccharide monooxygenases using highly-sensitive fluorimetric assay of the oxygen consumption rate. Carbohydr Res, 2017, 452: 156-161.

[50]

Hansson H, Karkehabadi S, Mikkelsen N, Douglas NR, Kim S, Lam A, Kaper T, Kelemen B, Meier KK, Jones SM, Solomon EI, Sandgren M. High-resolution structure of a lytic polysaccharide monooxygenase from Hypocrea jecorina reveals a predicted linker as an integral part of the catalytic domain. J Biol Chem, 2017, 292: 19099-19109.

[51]

Harris PV, Welner D, McFarland KC, Re E, Navarro Poulsen JC, Brown K, Salbo R, Ding H, Vlasenko E, Merino S, Xu F, Cherry J, Larsen S, Lo Leggio L. Stimulation of lignocellulosic biomass hydrolysis by proteins of glycoside hydrolase family 61: structure and function of a large, enigmatic family. Biochemistry, 2010, 49: 3305-3316.

[52]

Hegnar OA, Petrovic DM, Bissaro B, Alfredsen G, Várnai A, Eijsink VG. pH-dependent relationship between catalytic activity and hydrogen peroxide production shown via characterization of a lytic polysaccharide monooxygenase from Gloeophyllum trabeum. Appl Environ Microbiol, 2019, 85(5): e02612–18.

[53]

Hemsworth GR, Davies GJ, Walton PH. Recent insights into copper-containing lytic polysaccharide mono-oxygenases. Curr Opin Struct Biol, 2013, 23: 660-668.

[54]

Hemsworth GR, Taylor EJ, Kim RQ, Gregory RC, Lewis SJ, Turkenburg JP, Parkin A, Davies GJ, Walton PH. The copper active site of CBM33 polysaccharide oxygenases. J Am Chem Soc, 2013, 135: 6069-6077.

[55]

Hemsworth GR, Henrissat B, Davies GJ, Walton PH. Discovery and characterization of a new family of lytic polysaccharide monooxygenases. Nat Chem Biol, 2014, 10: 122-126.

[56]

Hemsworth GR, Johnston EM, Davies GJ, Walton PH. Lytic polysaccharide monooxygenases in biomass conversion. Trends Biotechnol, 2015, 33: 747-761.

[57]

Huttner S, Varnai A, Petrovic DM, Bach CX, Kim Anh DT, Thanh VN, Eijsink VGH, Larsbrink J, Olsson L. Specific xylan activity revealed for AA9 lytic polysaccharide monooxygenases of the thermophilic fungus Malbranchea cinnamomea by functional characterization. Appl Environ Microbiol, 2019

[58]

Isaksen T, Westereng B, Aachmann FL, Agger JW, Kracher D, Kittl R, Ludwig R, Haltrich D, Eijsink VG, Horn SJ. A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J Biol Chem, 2014, 289: 2632-2642.

[59]

Jagadeeswaran G, Gainey L, Prade R, Mort AJ. A family of AA9 lytic polysaccharide monooxygenases in Aspergillus nidulans is differentially regulated by multiple substrates and at least one is active on cellulose and xyloglucan. Appl Microbiol Biotechnol, 2016, 100: 4535-4547.

[60]

Jagadeeswaran G, Gainey L, Mort AJ. An AA9-LPMO containing a CBM1 domain in Aspergillus nidulans is active on cellulose and cleaves cello-oligosaccharides. AMB Express, 2018, 8: 171.

[61]

Jensen MS, Klinkenberg G, Bissaro B, Chylenski P, Vaaje-Kolstad G, Kvitvang HF, Naerdal GK, Sletta H, Forsberg Z, Eijsink VGH. Engineering chitinolytic activity into a cellulose-active lytic polysaccharide monooxygenase provides insights into substrate specificity. J Biol Chem, 2019, 294: 19349-19364.

[62]

Kadowaki MA, Varnai A, Jameson JK, Leite AE, Costa-Filho AJ, Kumagai PS, Prade RA, Polikarpov I, Eijsink VG. Functional characterization of a lytic polysaccharide monooxygenase from the thermophilic fungus Myceliophthora thermophila. PLoS ONE, 2018, 13(8): e0202148.

[63]

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: 144-154.

[64]

Karnaouri A, Muraleedharan MN, Dimarogona M, Topakas E, Rova U, Sandgren M, Christakopoulos P. Recombinant expression of thermostable processive MtEG5 endoglucanase and its synergism with MtLPMO from Myceliophthora thermophila during the hydrolysis of lignocellulosic substrates. Biotechnol Biofuels, 2017, 10: 126.

[65]

Kim IJ, Seo N, An HJ, Kim JH, Harris PV, Kim KH. Type-dependent action modes of TtAA9E and TaAA9A acting on cellulose and differently pretreated lignocellulosic substrates. Biotechnol Biofuels, 2017, 10: 46.

[66]

Kitaoku Y, Courtade G, Petrovic DM, Fukamizo T, Eijsink VGH, Aachmann FL. Resonance assignments for the apo-form of the cellulose-active lytic polysaccharide monooxygenase TaLPMO9A. Biomol NMR Assign, 2018, 12: 357-361.

[67]

Kittl R, Kracher D, Burgstaller D, Haltrich D, Ludwig R. Production of four Neurospora crassa lytic polysaccharide monooxygenases in Pichia pastoris monitored by a fluorimetric assay. Biotechnol Biofuels, 2012, 5: 79.

[68]

Kjaergaard CH, Qayyum MF, Wong SD, Xu F, Hemsworth GR, Walton DJ, Young NA, Davies GJ, Walton PH, Johansen KS, Hodgson KO, Hedman B, Solomon EI. Spectroscopic and computational insight into the activation of O2 by the mononuclear Cu center in polysaccharide monooxygenases. Proc Natl Acad Sci USA, 2014, 111: 8797-8802.

[69]

Kojima Y, Varnai A, Ishida T, Sunagawa N, Petrovic DM, Igarashi K, Jellison J, Goodell B, Alfredsen G, Westereng B, Eijsink VG, Yoshida M. 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, 2016, 82: 6557-6572.

[70]

Kracher D, Scheiblbrandner S, Felice AK, Breslmayr E, Preims M, Ludwicka K, Haltrich D, Eijsink VG, Ludwig R. Extracellular electron transfer systems fuel cellulose oxidative degradation. Science, 2016, 352: 1098-1101.

[71]

Kracher D, Andlar M, Furtmuller PG, Ludwig R. Active-site copper reduction promotes substrate binding of fungal lytic polysaccharide monooxygenase and reduces stability. J Biol Chem, 2018, 293: 1676-1687.

[72]

Kruer-Zerhusen N, Alahuhta M, Lunin VV, Himmel ME, Bomble YJ, Wilson DB. Structure of a Thermobifida fusca lytic polysaccharide monooxygenase and mutagenesis of key residues. Biotechnol Biofuels, 2017, 10: 243.

[73]

Ladeveze S, Haon M, Villares A, Cathala B, Grisel S, Herpoel-Gimbert I, Henrissat B, Berrin JG. The yeast Geotrichum candidum encodes functional lytic polysaccharide monooxygenases. Biotechnol Biofuels, 2017, 10: 215.

[74]

Laurent CV, Sun P, Scheiblbrandner S, Csarman F, Cannazza P, Frommhagen M, van Berkel WJ, Oostenbrink C, Kabel MA, Ludwig R. Influence of lytic polysaccharide monooxygenase active site segments on activity and affinity. Int J Mol Sci, 2019, 20(24): 6219.

[75]

Li X, Beeson WT IV, Phillips CM, Marletta MA, Cate JH. Structural basis for substrate targeting and catalysis by fungal polysaccharide monooxygenases. Structure, 2012, 20(6): 1051-1061.

[76]

Liu B, Olson A, Wu M, Broberg A, Sandgren M. Biochemical studies of two lytic polysaccharide monooxygenases from the white-rot fungus Heterobasidion irregulare and their roles in lignocellulose degradation. PLoS ONE, 2017, 12: e0189479.

[77]

Liu B, Kognole AA, Wu M, Westereng B, Crowley MF, Kim S, Dimarogona M, Payne CM, Sandgren M. Structural and molecular dynamics studies of a C1-oxidizing lytic polysaccharide monooxygenase from Heterobasidion irregulare reveal amino acids important for substrate recognition. FEBS J, 2018, 285: 2225-2242.

[78]

Lo Leggio L, Simmons TJ, Poulsen JC, Frandsen KE, Hemsworth GR, Stringer MA, von Freiesleben P, Tovborg M, Johansen KS, De Maria L, Harris PV, Soong CL, Dupree P, Tryfona T, Lenfant N, Henrissat B, Davies GJ, Walton PH. Structure and boosting activity of a starch-degrading lytic polysaccharide monooxygenase. Nat Commun, 2015, 6: 5961.

[79]

Lo Leggio L, Weihe CD, Poulsen JN, Sweeney M, Rasmussen F, Lin J, De Maria L, Wogulis M. Structure of a lytic polysaccharide monooxygenase from Aspergillus fumigatus and an engineered thermostable variant. Carbohydr Res, 2018, 469: 55-59.

[80]

Loose JS, Forsberg Z, Fraaije MW, Eijsink VG, Vaaje-Kolstad G. A rapid quantitative activity assay shows that the Vibrio cholerae colonization factor GbpA is an active lytic polysaccharide monooxygenase. FEBS Lett, 2014, 588: 3435-3440.

[81]

Manjeet K, Purushotham P, Neeraja C, Podile AR. Bacterial chitin binding proteins show differential substrate binding and synergy with chitinases. Microbiol Res, 2013, 168: 461-468.

[82]

Manjeet K, Madhuprakash J, Mormann M, Moerschbacher BM, Podile AR. A carbohydrate binding module-5 is essential for oxidative cleavage of chitin by a multi-modular lytic polysaccharide monooxygenase from Bacillus thuringiensis serovar kurstaki. Int J Biol Macromol, 2019, 127: 649-656.

[83]

Mekasha S, Forsberg Z, Dalhus B, Bacik JP, Choudhary S, Schmidt-Dannert C, Vaaje-Kolstad G, Eijsink VG. Structural and functional characterization of a small chitin-active lytic polysaccharide monooxygenase domain of a multi-modular chitinase from Jonesia denitrificans. FEBS Lett, 2016, 590: 34-42.

[84]

Mollers KB, Mikkelsen H, Simonsen TI, Cannella D, Johansen KS, Bjerrum MJ, Felby C. On the formation and role of reactive oxygen species in light-driven LPMO oxidation of phosphoric acid swollen cellulose. Carbohydr Res, 2017, 448: 182-186.

[85]

Muller G, Varnai A, Johansen KS, Eijsink VG, Horn SJ. Harnessing the potential of LPMO-containing cellulase cocktails poses new demands on processing conditions. Biotechnol Biofuels, 2015, 8: 187.

[86]

Mutahir Z, Mekasha S, Loose JSM, Abbas F, Vaaje-Kolstad G, Eijsink VGH, Forsberg Z. Characterization and synergistic action of a tetra-modular lytic polysaccharide monooxygenase from Bacillus cereus. FEBS Lett, 2018, 592: 2562-2571.

[87]

Nakagawa YS, Kudo M, Loose JS, Ishikawa T, Totani K, Eijsink VG, Vaaje-Kolstad G. A small lytic polysaccharide monooxygenase from Streptomyces griseus targeting alpha- and beta-chitin. FEBS J, 2015, 282: 1065-1079.

[88]

Nekiunaite L, Isaksen T, Vaaje-Kolstad G, Abou Hachem M. Fungal lytic polysaccharide monooxygenases bind starch and beta-cyclodextrin similarly to amylolytic hydrolases. FEBS Lett, 2016, 590: 2737-2747.

[89]

Nekiunaite L, Petrovic DM, Westereng B, Vaaje-Kolstad G, Hachem MA, Varnai A, Eijsink VG. FgLPMO9A from Fusarium graminearum cleaves xyloglucan independently of the backbone substitution pattern. FEBS Lett, 2016, 590: 3346-3356.

[90]

Paspaliari DK, Loose JS, Larsen MH, Vaaje-Kolstad G. Listeria monocytogenes has a functional chitinolytic system and an active lytic polysaccharide monooxygenase. FEBS J, 2015, 282: 921-936.

[91]

Patel I, Kracher D, Ma S, Garajova S, Haon M, Faulds CB, Berrin JG, Ludwig R, Record E. Salt-responsive lytic polysaccharide monooxygenases from the mangrove fungus Pestalotiopsis sp. NCi6. Biotechnol Biofuels, 2016, 9: 108.

[92]

Petrovic DM, Bissaro B, Chylenski P, Skaugen M, Sorlie M, Jensen MS, Aachmann FL, Courtade G, Varnai A, Eijsink VGH. Methylation of the N-terminal histidine protects a lytic polysaccharide monooxygenase from auto-oxidative inactivation. Protein Sci, 2018, 27: 1636-1650.

[93]

Petrovic DM, Varnai A, Dimarogona M, Mathiesen G, Sandgren M, Westereng B, Eijsink VGH. Comparison of three seemingly similar lytic polysaccharide monooxygenases from Neurospora crassa suggests different roles in plant biomass degradation. J Biol Chem, 2019, 294: 15068-15081.

[94]

Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen JC, Johansen KS, Krogh KB, Jorgensen CI, Tovborg M, Anthonsen A, Tryfona T, Walter CP, Dupree P, Xu F, Davies GJ, Walton PH. Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci USA, 2011, 108: 15079-15084.

[95]

Reese ET, Siu RG, Levinson HS. The biological degradation of soluble cellulose derivatives and its relationship to the mechanism of cellulose hydrolysis. J Bacteriol, 1950, 59: 485-497.

[96]

Russo DA, Zedler JAZ, Wittmann DN, Mollers B, Singh RK, Batth TS, van Oort B, Olsen JV, Bjerrum MJ, Jensen PE. Expression and secretion of a lytic polysaccharide monooxygenase by a fast-growing cyanobacterium. Biotechnol Biofuels, 2019, 12: 74.

[97]

Sabbadin F, Hemsworth GR, Ciano L, Henrissat B, Dupree P, Tryfona T, Marques RDS, Sweeney ST, Besser K, Elias L, Pesante G, Li Y, Dowle AA, Bates R, Gomez LD, Simister R, Davies GJ, Walton PH, Bruce NC, McQueen-Mason SJ. An ancient family of lytic polysaccharide monooxygenases with roles in arthropod development and biomass digestion. Nat Commun, 2018, 9: 756.

[98]

Shukla AK, Upadhyay SK, Mishra M, Saurabh S, Singh R, Singh H, Thakur N, Rai P, Pandey P, Hans AL, Srivastava S, Rajapure V, Yadav SK, Singh MK, Kumar J, Chandrashekar K, Verma PC, Singh AP, Nair KN, Bhadauria S, Wahajuddin M, Singh S, Sharma S, Omkar, Upadhyay RS, Ranade SA, Tuli R, Singh PK. Expression of an insecticidal fern protein in cotton protects against whitefly. Nat Biotechnol, 2016, 34: 1046-1051.

[99]

Simmons TJ, Frandsen KEH, Ciano L, Tryfona T, Lenfant N, Poulsen JC, Wilson LFL, Tandrup T, Tovborg M, Schnorr K, Johansen KS, Henrissat B, Walton PH, Lo Leggio L, Dupree P. Structural and electronic determinants of lytic polysaccharide monooxygenase reactivity on polysaccharide substrates. Nat Commun, 2017, 8: 1064.

[100]

Singh RK, Blossom BM, Russo DA, Singh R, Weihe H, Andersen NH, Tiwari MK, Jensen PE, Felby C, Bjerrum MJ. Detection and characterization of a novel copper-dependent intermediate in a lytic polysaccharide monooxygenase. Eur J, 2020, 26(2): 454-463.

[101]

Span EA, Marletta MA. The framework of polysaccharide monooxygenase structure and chemistry. Curr Opin Struct Biol, 2015, 35: 93-99.

[102]

Span EA, Suess DLM, Deller MC, Britt RD, Marletta MA. The role of the secondary coordination sphere in a fungal polysaccharide monooxygenase. ACS Chem Biol, 2017, 12: 1095-1103.

[103]

Tan TC, Kracher D, Gandini R, Sygmund C, Kittl R, Haltrich D, Hallberg BM, Ludwig R, Divne C. Structural basis for cellobiose dehydrogenase action during oxidative cellulose degradation. Nat Commun, 2015, 6: 7542.

[104]

Tandrup T, Frandsen KEH, Johansen KS, Berrin JG, Lo Leggio L. Recent insights into lytic polysaccharide monooxygenases (LPMOs). Biochem Soc Trans, 2018, 46: 1431-1447.

[105]

Tanghe M, Danneels B, Camattari A, Glieder A, Vandenberghe I, Devreese B, Stals I, Desmet T. Recombinant Expression of Trichoderma reesei Cel61A in Pichia pastoris: optimizing Yield and N-terminal Processing. Mol Biotechnol, 2015, 57: 1010-1017.

[106]

Vaaje-Kolstad G, Horn SJ, van Aalten DM, Synstad B, Eijsink VG. The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem, 2005, 280: 28492-28497.

[107]

Vaaje-Kolstad G, Houston DR, Riemen AH, Eijsink VG, van Aalten DM. Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J Biol Chem, 2005, 280: 11313-11319.

[108]

Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sørlie M, Eijsink VG. An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science, 2010, 330(6001): 219-222.

[109]

Vaaje-Kolstad G, Bohle LA, Gaseidnes S, Dalhus B, Bjoras M, Mathiesen G, Eijsink VG. Characterization of the chitinolytic machinery of Enterococcus faecalis V583 and high-resolution structure of its oxidative CBM33 enzyme. J Mol Biol, 2012, 416: 239-254.

[110]

Vaaje-Kolstad G, Forsberg Z, Loose JS, Bissaro B, Eijsink VG. Structural diversity of lytic polysaccharide monooxygenases. Curr Opin Struct Biol, 2017, 44: 67-76.

[111]

Valenzuela SV, Ferreres G, Margalef G, Pastor FIJ. Fast purification method of functional LPMOs from Streptomyces ambofaciens by affinity adsorption. Carbohydr Res, 2017, 448: 205-211.

[112]

Várnai A, Umezawa K, Yoshida M, Eijsink VG. The pyrroloquinoline-quinone-dependent pyranose dehydrogenase from Coprinopsis cinerea drives lytic polysaccharide monooxygenase action. Appl Environ Microbiol, 2018, 84(11): e00156–18.

[113]

Villares A, Moreau C, Bennati-Granier C, Garajova S, Foucat L, Falourd X, Saake B, Berrin JG, Cathala B. Lytic polysaccharide monooxygenases disrupt the cellulose fibers structure. Sci Rep, 2017, 7: 40262.

[114]

Vu VV, Beeson WT, Phillips CM, Cate JH, Marletta MA. Determinants of regioselective hydroxylation in the fungal polysaccharide monooxygenases. J Am Chem Soc, 2014, 136: 562-565.

[115]

Vu VV, Beeson WT, Span EA, Farquhar ER, Marletta MA. A family of starch-active polysaccharide monooxygenases. Proc Natl Acad Sci USA, 2014, 111: 13822-13827.

[116]

Vu VV, Hangasky JA, Detomasi TC, Henry SJW, Ngo ST, Span EA, Marletta MA. Substrate selectivity in starch polysaccharide monooxygenases. J Biol Chem, 2019, 294: 12157-12166.

[117]

Vuong TV, Liu B, Sandgren M, Master ER. Microplate-based detection of lytic polysaccharide monooxygenase activity by fluorescence-labeling of insoluble oxidized products. Biomacromolecules, 2017, 18: 610-616.

[118]

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

[119]

Wang D, Li J, Wong ACY, Aachmann FL, Hsieh YSY. A colorimetric assay to rapidly determine the activities of lytic polysaccharide monooxygenases. Biotechnol Biofuels, 2018, 11: 215.

[120]

Westereng B, Ishida T, Vaaje-Kolstad G, Wu M, Eijsink VG, Igarashi K, Samejima M, Stahlberg J, Horn SJ, Sandgren M. The putative endoglucanase PcGH61D from Phanerochaete chrysosporium is a metal-dependent oxidative enzyme that cleaves cellulose. PLoS ONE, 2011, 6: e27807.

[121]

Westereng B, Agger JW, Horn SJ, Vaaje-Kolstad G, Aachmann FL, Stenstrom YH, Eijsink VG. Efficient separation of oxidized cello-oligosaccharides generated by cellulose degrading lytic polysaccharide monooxygenases. J Chromatogr A, 2013, 1271: 144-152.

[122]

Westereng B, Cannella D, Wittrup Agger J, Jorgensen H, Larsen Andersen M, Eijsink VG, Felby C. Enzymatic cellulose oxidation is linked to lignin by long-range electron transfer. Sci Rep, 2015, 5: 18561.

[123]

Westereng B, Arntzen MO, Aachmann FL, Varnai A, Eijsink VG, Agger JW. Simultaneous analysis of C1 and C4 oxidized oligosaccharides, the products of lytic polysaccharide monooxygenases acting on cellulose. J Chromatogr A, 2016, 1445: 46-54.

[124]

Wong E, Vaaje-Kolstad G, Ghosh A, Hurtado-Guerrero R, Konarev PV, Ibrahim AF, Svergun DI, Eijsink VG, Chatterjee NS, van Aalten DM. The Vibrio cholerae colonization factor GbpA possesses a modular structure that governs binding to different host surfaces. PLoS Pathog, 2012, 8: e1002373.

[125]

Wu M, Beckham GT, Larsson AM, Ishida T, Kim S, Payne CM, Himmel ME, Crowley MF, Horn SJ, Westereng B, Igarashi K, Samejima M, Stahlberg J, Eijsink VG, Sandgren M. Crystal structure and computational characterization of the lytic polysaccharide monooxygenase GH61D from the Basidiomycota fungus Phanerochaete chrysosporium. J Biol Chem, 2013, 288: 12828-12839.

[126]

Yadav SK, Archana, Singh R, Singh PK, Vasudev PG. Insecticidal fern protein Tma12 is possibly a lytic polysaccharide monooxygenase. Planta, 2019, 249(6): 1987-1996.

[127]

Zhang H, Zhao Y, Cao H, Mou G, Yin H. Expression and characterization of a lytic polysaccharide monooxygenase from Bacillus thuringiensis. Int J Biol Macromol, 2015, 79: 72-75.

[128]

Zhang R, Liu Y, Zhang Y, Feng D, Hou S, Guo W, Niu K, Jiang Y, Han L, Sindhu L, Fang X. Identification of a thermostable fungal lytic polysaccharide monooxygenase and evaluation of its effect on lignocellulosic degradation. Appl Microbiol Biotechnol, 2019, 103: 5739-5750.

[129]

Zhou H, Li T, Yu Z, Ju J, Zhang H, Tan H, Li K, Yin H. A lytic polysaccharide monooxygenase from Myceliophthora thermophila and its synergism with cellobiohydrolases in cellulose hydrolysis. Int J Biol Macromol, 2019, 139: 570-576.

[130]

Zhou X, Qi X, Huang H, Zhu H. Sequence and structural analysis of AA9 and AA10 LPMOs: an insight into the basis of substrate specificity and regioselectivity. Int J Mol Sci, 2019, 20(18): 4594.

Funding

Guangdong Province Science and Technology Innovation Strategy Special Fund(2018B020206001)

the GDAS’ Special Project of Science and Technology Development(2018GDASCX-0909)

the Science and Technology Plan Project of Guangdong Province(2016A010105013)

National Natural Science Foundation of China(31400681)

AI Summary AI Mindmap
PDF

132

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/