Revisiting the AA14 family of lytic polysaccharide monooxygenases and their catalytic activity.
AA14
LPMO
auxiliary activity
lytic polysaccharide monooxygenase
xylan
Journal
FEBS letters
ISSN: 1873-3468
Titre abrégé: FEBS Lett
Pays: England
ID NLM: 0155157
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
08
06
2023
received:
31
03
2023
accepted:
26
06
2023
medline:
23
8
2023
pubmed:
7
7
2023
entrez:
7
7
2023
Statut:
ppublish
Résumé
Lytic polysaccharide monooxygenases (LPMOs) belonging to the AA14 family are believed to contribute to the enzymatic degradation of lignocellulosic biomass by specifically acting on xylan in recalcitrant cellulose-xylan complexes. Functional characterization of an AA14 LPMO from Trichoderma reesei, TrAA14A, and a re-evaluation of the properties of the previously described AA14 from Pycnoporus coccineus, PcoAA14A, showed that these proteins have oxidase and peroxidase activities that are common for LPMOs. However, we were not able to detect activity on cellulose-associated xylan or any other tested polysaccharide substrate, meaning that the substrate of these enzymes remains unknown. Next to raising questions regarding the true nature of AA14 LPMOs, the present data illustrate possible pitfalls in the functional characterization of these intriguing enzymes.
Identifiants
pubmed: 37418595
doi: 10.1002/1873-3468.14694
doi:
Substances chimiques
Mixed Function Oxygenases
EC 1.-
Xylans
0
Polysaccharides
0
Cellulose
9004-34-6
Oxidoreductases
EC 1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2086-2102Informations de copyright
© 2023 The Authors. FEBS Letters published by John Wiley & Sons Ltd on behalf of Federation of European Biochemical Societies.
Références
van der Wal A, Geydan TD, Kuyper TW and de Boer W (2013) A thready affair: linking fungal diversity and community dynamics to terrestrial decomposition processes. FEMS Microbiol Rev 37, 477-494.
Drula E, Garron M-L, Dogan S, Lombard V, Henrissat B and Terrapon N (2022) The carbohydrate-active enzyme database: functions and literature. Nucleic Acids Res 50, D571-D577.
Vaaje-Kolstad G, Westereng B, Horn SJ, Liu Z, Zhai H, Sørlie M and Eijsink VGH (2010) An oxidative enzyme boosting the enzymatic conversion of recalcitrant polysaccharides. Science 330, 219-222.
Horn SJ, Vaaje-Kolstad G, Westereng B and Eijsink VGH (2012) Novel enzymes for the degradation of cellulose. Biotechnol Biofuels 5, 45.
Beeson WT, Vu VV, Span EA, Phillips CM and Marletta MA (2015) Cellulose degradation by polysaccharide monooxygenases. Annu Rev Biochem 84, 923-946.
Chylenski P, Bissaro B, Sørlie M, Røhr ÅK, Várnai A, Horn SJ and Eijsink VGH (2019) Lytic polysaccharide monooxygenases in enzymatic processing of lignocellulosic biomass. ACS Catal 9, 4970-4991.
Walton PH and Davies GJ (2016) On the catalytic mechanisms of lytic polysaccharide monooxygenases. Curr Opin Chem Biol 31, 195-207.
Quinlan RJ, Sweeney MD, Lo Leggio L, Otten H, Poulsen J-CN, Johansen KS, Krogh KBRM, Jørgensen CI, Tovborg M, Anthonsen A et al. (2011) Insights into the oxidative degradation of cellulose by a copper metalloenzyme that exploits biomass components. Proc Natl Acad Sci U S A 108, 15079-15084.
Langston JA, Shaghasi T, Abbate E, Xu F, Vlasenko E and Sweeney MD (2011) Oxidoreductive cellulose depolymerization by the enzymes cellobiose dehydrogenase and glycoside hydrolase 61. Appl Environ Microbiol 77, 7007-7015.
Phillips CM, Beeson WT, Cate JH and Marletta MA (2011) Cellobiose dehydrogenase and a copper-dependent polysaccharide monooxygenase potentiate cellulose degradation by Neurospora crassa. ACS Chem Biol 6, 1399-1406.
Hu J, Arantes V, Pribowo A, Gourlay K and Saddler JN (2014) Substrate factors that influence the synergistic interaction of AA9 and cellulases during the enzymatic hydrolysis of biomass. Energ Environ Sci 7, 2308-2315.
Westereng B, Cannella D, Agger JW, Jørgensen H, Andersen ML, Eijsink VGH and Felby C (2015) Enzymatic cellulose oxidation is linked to lignin by long-range electron transfer. Sci Rep 5, 18561.
Kracher D, Scheiblbrandner S, Felice AKG, Breslmayr E, Preims M, Ludwicka K, Haltrich D, Eijsink VGH and Ludwig R (2016) Extracellular electron transfer systems fuel cellulose oxidative degradation. Science 352, 1098-1101.
Haddad Momeni M, Fredslund F, Bissaro B, Raji O, Vuong TV, Meier S, Nielsen TS, Lombard V, Guigliarelli B, Biaso F et al. (2021) Discovery of fungal oligosaccharide-oxidising flavo-enzymes with previously unknown substrates, redox-activity profiles and interplay with LPMOs. Nat Commun 12, 2132.
Frommhagen M, Westphal AH, van Berkel WJH and Kabel MA (2018) Distinct substrate specificities and electron-donating systems of fungal lytic polysaccharide monooxygenases. Front Microbiol 9, 1080.
Garajova S, Mathieu Y, Beccia MR, Bennati-Granier C, Biaso F, Fanuel M, Ropartz D, Guigliarelli B, Record E, Rogniaux H et al. (2016) Single-domain flavoenzymes trigger lytic polysaccharide monooxygenases for oxidative degradation of cellulose. Sci Rep 6, 28276.
Bissaro B, Røhr ÅK, Müller G, Chylenski P, Skaugen M, Forsberg Z, Horn SJ, Vaaje-Kolstad G and Eijsink VGH (2017) Oxidative cleavage of polysaccharides by monocopper enzymes depends on H2O2. Nat Chem Biol 13, 1123-1128.
Bissaro B and Eijsink VGH (2023) Lytic polysaccharide monooxygenases: enzymes for controlled and site-specific Fenton-like chemistry. Essays Biochem 67, 575-584.
Kuusk S, Bissaro B, Kuusk P, Forsberg Z, Eijsink VGH, Sørlie M and Väljamäe P (2018) Kinetics of H2O2-driven degradation of chitin by a bacterial lytic polysaccharide monooxygenase. J Biol Chem 293, 523-531.
Kont R, Bissaro B, Eijsink VGH and Väljamäe P (2020) Kinetic insights into the peroxygenase activity of cellulose-active lytic polysaccharide monooxygenases (LPMOs). Nat Commun 11, 5786.
Hedison TM, Breslmayr E, Shanmugam M, Karnpakdee K, Heyes DJ, Green AP, Ludwig R, Scrutton NS and Kracher D (2021) Insights into the H2O2-driven catalytic mechanism of fungal lytic polysaccharide monooxygenases. FEBS J 288, 4115-4128.
Chang H, Gacias Amengual N, Botz A, Schwaiger L, Kracher D, Scheiblbrandner S, Csarman F and Ludwig R (2022) Investigating lytic polysaccharide monooxygenase-assisted wood cell wall degradation with microsensors. Nat Commun 13, 6258.
Forsberg Z, Vaaje-Kolstad G, Westereng B, Bunaes AC, Stenstrøm Y, MacKenzie A, Sørlie M, Horn SJ and Eijsink VGH (2011) Cleavage of cellulose by a CBM33 protein. Protein Sci 20, 1479-1483.
Agger JW, Isaksen T, Várnai A, Vidal-Melgosa S, Willats WGT, Ludwig R, Horn SJ, Eijsink VGH and Westereng B (2014) Discovery of LPMO activity on hemicelluloses shows the importance of oxidative processes in plant cell wall degradation. Proc Natl Acad Sci U S A 111, 6287-6292.
Bennati-Granier C, Garajova S, Champion C, Grisel S, Haon M, Zhou S, Fanuel M, Ropartz D, Rogniaux H, Gimbert I et al. (2015) Substrate specificity and regioselectivity of fungal AA9 lytic polysaccharide monooxygenases secreted by Podospora anserina. Biotechnol Biofuels 8, 90.
Fanuel M, Garajova S, Ropartz D, McGregor N, Brumer H, Rogniaux H and Berrin J-G (2017) The Podospora anserina lytic polysaccharide monooxygenase PaLPMO9H catalyzes oxidative cleavage of diverse plant cell wall matrix glycans. Biotechnol Biofuels 10, 63.
Petrović DM, Várnai A, Dimarogona M, Mathiesen G, Sandgren M, Westereng B and Eijsink VGH (2019) Comparison of three seemingly similar lytic polysaccharide monooxygenases from Neurospora crassa suggests different roles in plant biomass degradation. J Biol Chem 294, 15068-15081.
Frommhagen M, Sforza S, Westphal AH, Visser J, Hinz SW, Koetsier MJ, van Berkel WJ, Gruppen H and Kabel MA (2015) Discovery of the combined oxidative cleavage of plant xylan and cellulose by a new fungal polysaccharide monooxygenase. Biotechnol Biofuels 8, 101.
Hüttner S, Várnai A, Petrović DM, Bach CX, Kim Anh DT, Thanh VN, Eijsink VGH, Larsbrink J and Olsson L (2019) Specific xylan activity revealed for AA9 lytic polysaccharide monooxygenases of the thermophilic fungus Malbranchea cinnamomea by functional characterization. Appl Environ Microbiol 85, e01408-19.
Hegnar OA, Østby H, Petrović DM, Olsson L, Várnai A and Eijsink VGH (2021) Quantifying oxidation of cellulose-associated glucuronoxylan by two lytic polysaccharide monooxygenases from Neurospora crassa. Appl Environ Microbiol 87, e01652-21.
Isaksen T, Westereng B, Aachmann FL, Agger JW, Kracher D, Kittl R, Ludwig R, Haltrich D, Eijsink VG and Horn SJ (2014) A C4-oxidizing lytic polysaccharide monooxygenase cleaving both cellulose and cello-oligosaccharides. J Biol Chem 289, 2632-2642.
Várnai A, Hegnar OA, Horn SJ, Eijsink VGH and Berrin J-G (2021) Fungal lytic polysaccharide monooxygenases (LPMOs): biological importance and applications. In Encyclopedia of Mycology (Zaragoza Ó and Casadevall A, eds), pp. 281-294. Elsevier, Oxford.
Sabbadin F, Urresti S, Henrissat B, Avrova AO, Welsh LRJ, Lindley PJ, Csukai M, Squires JN, Walton PH, Davies GJ et al. (2021) Secreted pectin monooxygenases drive plant infection by pathogenic oomycetes. Science 373, 774-779.
Nagy LG, Riley R, Tritt A, Adam C, Daum C, Floudas D, Sun H, Yadav JS, Pangilinan J, Larsson KH et al. (2016) Comparative genomics of early-diverging mushroom-forming fungi provides insights into the origins of lignocellulose decay capabilities. Mol Biol Evol 33, 959-970.
Fogelqvist J, Tzelepis G, Bejai S, Ilbäck J, Schwelm A and Dixelius C (2018) Analysis of the hybrid genomes of two field isolates of the soil-borne fungal species Verticillium longisporum. BMC Genomics 19, 14.
Carpita NC and McCann MC (2020) Redesigning plant cell walls for the biomass-based bioeconomy. J Biol Chem 295, 15144-15157.
Bissaro B, Várnai A, Røhr ÅK and Eijsink VGH (2018) Oxidoreductases and reactive oxygen species in conversion of lignocellulosic biomass. Microbiol Mol Biol Rev 82, e00029-18.
Couturier M, Ladeveze S, Sulzenbacher G, Ciano L, Fanuel M, Moreau C, Villares A, Cathala B, Chaspoul F, Frandsen KE et al. (2018) Lytic xylan oxidases from wood-decay fungi unlock biomass degradation. Nat Chem Biol 14, 306-310.
Nekiunaite L, Petrović DM, Westereng B, Vaaje-Kolstad G, Hachem MA, Várnai A and Eijsink VGH (2016) FgLPMO9A from Fusarium graminearum cleaves xyloglucan independently of the backbone substitution pattern. FEBS Lett 590, 3346-3356.
Vandhana TM, Reyre J-L, Sushmaa D, Berrin J-G, Bissaro B and Madhuprakash J (2022) On the expansion of biological functions of lytic polysaccharide monooxygenases. New Phytol 233, 2380-2396.
Rieder L, Petrović D, Väljamäe P, Eijsink VGH and Sørlie M (2021) Kinetic characterization of a putatively chitin-active LPMO reveals a preference for soluble substrates and absence of monooxygenase activity. ACS Catal 11, 11685-11695.
Zhong X, Zhang L, van Wezel Gilles P, Vijgenboom E and Claessen D (2022) Role for a lytic polysaccharide monooxygenase in cell wall remodeling in Streptomyces coelicolor. MBio 13, e00456-22.
Askarian F, Uchiyama S, Masson H, Sørensen HV, Golten O, Bunaes AC, Mekasha S, Røhr ÅK, Kommedal E, Ludviksen JA et al. (2021) The lytic polysaccharide monooxygenase CbpD promotes Pseudomonas aeruginosa virulence in systemic infection. Nat Commun 12, 1230.
Sabbadin F, Henrissat B, Bruce NC and McQueen-Mason SJ (2021) Lytic polysaccharide monooxygenases as chitin-specific virulence factors in crayfish plague. Biomolecules 11, 1180.
Zerva A, Pentari C, Grisel S, Berrin J-G and Topakas E (2020) A new synergistic relationship between xylan-active LPMO and xylobiohydrolase to tackle recalcitrant xylan. Biotechnol Biofuels 13, 142.
Vaaje-Kolstad G, Horn SJ, van Aalten DMF, Synstad B and Eijsink VGH (2005) The non-catalytic chitin-binding protein CBP21 from Serratia marcescens is essential for chitin degradation. J Biol Chem 280, 28492-28497.
Chylenski P, Petrović DM, Müller G, Dahlström M, Bengtsson O, Lersch M, Siika-Aho M, Horn SJ and Eijsink VGH (2017) Enzymatic degradation of sulfite-pulped softwoods and the role of LPMOs. Biotechnol Biofuels 10, 177.
Vaaje-Kolstad G, Houston DR, Riemen AHK, Eijsink VGH and van Aalten DMF (2005) Crystal structure and binding properties of the Serratia marcescens chitin-binding protein CBP21. J Biol Chem 280, 11313-11319.
Kittl R, Kracher D, Burgstaller D, Haltrich D and Ludwig R (2012) Production of four Neurospora crassa lytic polysaccharide monooxygenases in Pichia pastoris monitored by a fluorimetric assay. Biotechnol Biofuels 5, 79.
Gasteiger E, Hoogland C, Gattiker A, Duvaud SE, Wilkins MR, Appel RD and Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook (Walker JM, ed.), pp. 571-607. Humana Press, Totowa, NJ.
Wood TM (1988) Preparation of crystalline, amorphous, and dyed cellulase substrates. Methods Enzymol 160, 19-25.
Rødsrud G, Lersch M and Sjöde A (2012) History and future of world's most advanced biorefinery in operation. Biomass Bioenergy 46, 46-59.
Kalyani DC, Zamanzadeh M, Müller G and Horn SJ (2017) Biofuel production from birch wood by combining high solid loading simultaneous saccharification and fermentation and anaerobic digestion. Appl Energy 193, 210-219.
Huynh K and Partch CL (2015) Analysis of protein stability and ligand interactions by thermal shift assay. Curr Protoc Protein Sci 79, 28.9.1-28.9.14.
Breslmayr E, Hanžek M, Hanrahan A, Leitner C, Kittl R, Šantek B, Oostenbrink C and Ludwig R (2018) A fast and sensitive activity assay for lytic polysaccharide monooxygenase. Biotechnol Biofuels 11, 79.
Zamocky M, Schumann C, Sygmund C, O'Callaghan J, Dobson AD, Ludwig R, Haltrich D and Peterbauer CK (2008) Cloning, sequence analysis and heterologous expression in Pichia pastoris of a gene encoding a thermostable cellobiose dehydrogenase from Myriococcum thermophilum. Protein Expr Purif 59, 258-265.
Westereng B, Agger JW, Horn SJ, Vaaje-Kolstad G, Aachmann FL, Stenstrøm YH and Eijsink VG (2013) Efficient separation of oxidized cello-oligosaccharides generated by cellulose degrading lytic polysaccharide monooxygenases. J Chromatogr A 1271, 144-152.
Jumper J, Evans R, Pritzel A, Green T, Figurnov M, Ronneberger O, Tunyasuvunakool K, Bates R, Žídek A, Potapenko A et al. (2021) Highly accurate protein structure prediction with AlphaFold. Nature 596, 583-589.
Hebditch M and Warwicker J (2019) Web-based display of protein surface and pH-dependent properties for assessing the developability of biotherapeutics. Sci Rep 9, 1969.
Huang Y, Niu B, Gao Y, Fu L and Li W (2010) CD-HIT suite: a web server for clustering and comparing biological sequences. Bioinformatics 26, 680-682.
Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W and Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59, 307-321.
Whelan S and Goldman N (2001) A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18, 691-699.
Lefort V, Longueville J-E and Gascuel O (2017) SMS: smart model selection in PhyML. Mol Biol Evol 34, 2422-2424.
Letunic I and Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49, W293-W296.
Schwaiger L, Zenone A, Csarman F and Ludwig R (2023) Continuous photometric activity assays for lytic polysaccharide monooxygenase-critical assessment and practical considerations. Methods Enzymol 679, 381-404.
Stepnov AA and Eijsink VGH (2023) Looking at LPMO reactions through the lens of the HRP/Amplex red assay. Methods Enzymol 679, 163-189.
Stepnov AA, Christensen IA, Forsberg Z, Aachmann FL, Courtade G and Eijsink VGH (2022) The impact of reductants on the catalytic efficiency of a lytic polysaccharide monooxygenase and the special role of dehydroascorbic acid. FEBS Lett 596, 53-70.
Stepnov AA, Eijsink VGH and Forsberg Z (2022) Enhanced in situ H2O2 production explains synergy between an LPMO with a cellulose-binding domain and a single-domain LPMO. Sci Rep 12, 6129.
Stepnov AA, Forsberg Z, Sørlie M, Nguyen GS, Wentzel A, Røhr Å and Eijsink VGH (2021) Unraveling the roles of the reductant and free copper ions in LPMO kinetics. Biotechnol Biofuels 14, 28.
Rieder L, Stepnov AA, Sørlie M and Eijsink VGH (2021) Fast and specific peroxygenase reactions catalyzed by fungal mono-copper enzymes. Biochemistry 60, 3633-3643.
Bissaro B, Kommedal E, Røhr ÅK and Eijsink VGH (2020) Controlled depolymerization of cellulose by light-driven lytic polysaccharide oxygenases. Nat Commun 11, 890.
Zhang J, Presley GN, Hammel KE, Ryu JS, Menke JR, Figueroa M, Hu D, Orr G and Schilling JS (2016) Localizing gene regulation reveals a staggered wood decay mechanism for the brown rot fungus Postia placenta. Proc Natl Acad Sci U S A 113, 10968-10973.
Jurak E, Suzuki H, van Erven G, Gandier JA, Wong P, Chan K, Ho CY, Gong Y, Tillier E, Rosso MN et al. (2018) Dynamics of the Phanerochaete carnosa transcriptome during growth on aspen and spruce. BMC Genomics 19, 815.
Muraguchi H, Umezawa K, Niikura M, Yoshida M, Kozaki T, Ishii K, Sakai K, Shimizu M, Nakahori K, Sakamoto Y et al. (2015) Strand-specific RNA-seq analyses of fruiting body development in Coprinopsis cinerea. PloS One 10, e0141586.
Couturier M, Navarro D, Chevret D, Henrissat B, Piumi F, Ruiz-Dueñas FJ, Martinez AT, Grigoriev IV, Riley R, Lipzen A et al. (2015) Enhanced degradation of softwood versus hardwood by the white-rot fungus Pycnoporus coccineus. Biotechnol Biofuels 8, 216.
Miyauchi S, Hage H, Drula E, Lesage-Meessen L, Berrin J-G, Navarro D, Favel A, Chaduli D, Grisel S, Haon M et al. (2020) Conserved white-rot enzymatic mechanism for wood decay in the Basidiomycota genus Pycnoporus. DNA Res 27, dsaa011.
Tamburrini KC, Terrapon N, Lombard V, Bissaro B, Longhi S and Berrin J-G (2021) Bioinformatic analysis of lytic polysaccharide monooxygenases reveals the pan-families occurrence of intrinsically disordered C-terminal extensions. Biomolecules 11, 1632.
Tõlgo M, Hegnar OA, Østby H, Várnai A, Vilaplana F, Eijsink VGH and Olsson L (2022) Comparison of six lytic polysaccharide monooxygenases from Thermothielavioides terrestris shows that functional variation underlies the multiplicity of LPMO genes in filamentous fungi. Appl Environ Microbiol 88, e00096-22.
Eijsink VGH, Petrović D, Forsberg Z, Mekasha S, Røhr AK, Várnai A, Bissaro B and Vaaje-Kolstad G (2019) On the functional characterization of lytic polysaccharide monooxygenases (LPMOs). Biotechnol Biofuels 12, 58.
Busse-Wicher M, Li A, Silveira RL, Pereira CS, Tryfona T, Gomes TCF, Skaf MS and Dupree P (2016) Evolution of xylan substitution patterns in gymnosperms and angiosperms: implications for xylan interaction with cellulose. Plant Physiol 171, 2418-2431.
Busse-Wicher M, Grantham NJ, Lyczakowski JJ, Nikolovski N and Dupree P (2016) Xylan decoration patterns and the plant secondary cell wall molecular architecture. Biochem Soc Trans 44, 74-78.
Zhou P, Zhang J, Zhang Y, Liu Y, Liang J, Liu B and Zhang W (2016) Generation of hydrogen peroxide and hydroxyl radical resulting from oxygen-dependent oxidation of L-ascorbic acid via copper redox-catalyzed reactions. RSC Adv 6, 38541-38547.
Kachur AV, Koch CJ and Biaglow JE (1999) Mechanism of copper-catalyzed autoxidation of cysteine. Free Radic Res 31, 23-34.
Labourel A, Frandsen KEH, Zhang F, Brouilly N, Grisel S, Haon M, Ciano L, Ropartz D, Fanuel M, Martin F et al. (2020) A fungal family of lytic polysaccharide monooxygenase-like copper proteins. Nat Chem Biol 16, 345-350.
Filiatrault-Chastel C, Navarro D, Haon M, Grisel S, Herpoël-Gimbert I, Chevret D, Fanuel M, Henrissat B, Heiss-Blanquet S, Margeot A et al. (2019) AA16, a new lytic polysaccharide monooxygenase family identified in fungal secretomes. Biotechnol Biofuels 12, 55.
Sun P, Huang Z, Banerjee S, Kadowaki MAS, Veersma RJ, Magri S, Hilgers R, Muderspach SJ, Laurent CVFP, Ludwig R et al. (2023) AA16 oxidoreductases boost cellulose-active AA9 lytic polysaccharide monooxygenases from Myceliophthora thermophila. ACS Catal 13, 4454-4467.
Gonçalves AP, Heller J, Span EA, Rosenfield G, Do HP, Palma-Guerrero J, Requena N, Marletta MA and Glass NL (2019) Allorecognition upon fungal cell-cell contact determines social cooperation and impacts the acquisition of multicellularity. Curr Biol 29, 3006-3017.e3.