Fungal lignin peroxidase does not produce the veratryl alcohol cation radical as a diffusible ligninolytic oxidant

Houtman, Carl J.; Maligaspe, Eranda; Hunt, Christopher G.; Fernández-Fueyo, Elena; Martínez, Angel T.; Hammel, Kenneth E.

doi:10.1074/jbc.RA117.001153

Title: Fungal lignin peroxidase does not produce the veratryl alcohol cation radical as a diffusible ligninolytic oxidant

Journal Article · Thu Mar 01 00:00:00 EST 2018 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.RA117.001153· OSTI ID:1761547

Houtman, Carl J.; Maligaspe, Eranda; Hunt, Christopher G.; Fernández-Fueyo, Elena; Martínez, Angel T.; Hammel, Kenneth E.

Peroxidases are considered essential agents of lignin degradation by white-rot basidiomycetes. However, low-molecular-weight oxidants likely have a primary role in lignin breakdown because many of these fungi delignify wood before its porosity has sufficiently increased for enzymes to infiltrate. It has been proposed that lignin peroxidases (LiPs, EC 1.11.1.14) fulfill this role by oxidizing the secreted fungal metabolite veratryl alcohol (VA) to its aryl cation radical (VA^+•), releasing it to act as a one-electron lignin oxidant within woody plant cell walls. Here, we attached the fluorescent oxidant sensor BODIPY 581/591 throughout beads with a nominal porosity of 6 kDa and assessed whether peroxidase-generated aryl cation radical systems could oxidize the beads. As positive control, we used the 1,2,4,5-tetramethoxybenzene (TMB) cation radical, generated from TMB by horseradish peroxidase. This control oxidized the beads to depths that increased with the amount of oxidant supplied, ultimately resulting in completely oxidized beads. A reaction–diffusion computer model yielded oxidation profiles that were within the 95% confidence intervals for the data. By contrast, bead oxidation caused by VA and the LiPA isozyme of Phanerochaete chrysosporium was confined to a shallow shell of LiP-accessible volume at the bead surface, regardless of how much oxidant was supplied. This finding contrasted with the modeling results, which showed that if the LiP/VA system were to release VA^+•, it would oxidize the bead interiors. Finally, we conclude that LiPA releases insignificant quantities of VA^+• and that a different mechanism produces small ligninolytic oxidants during white rot.

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Research Organization:: Univ. of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0006929

OSTI ID:: 1761547

Alternate ID(s):: OSTI ID: 1540309

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 293 Journal Issue: 13; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 19 works

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References (54)

Substrate-dependent changes of the oxidative O-dealkylation mechanism of several chemical and biological oxidizing systems Urano, Yasuteru; Higuchi, Tsunehiko; Hirobe, Masaaki Journal of the Chemical Society, Perkin Transactions 2, Issue 6 https://doi.org/10.1039/p29960001169	journal	January 1996
Oxidation of 1,2,4,5-Tetramethoxybenzene by Lignin Peroxidase ofPhanerochaete chrysosporium Koduri, Rao S.; Whitwam, Ross E.; Barr, David Archives of Biochemistry and Biophysics, Vol. 326, Issue 2 https://doi.org/10.1006/abbi.1996.0074	journal	February 1996
Pre-steady-state kinetic study on the formation of Compound I and II of ligninase Harvey, Patricia J.; Palmer, John M.; Schoemaker, Hans E. Biochimica et Biophysica Acta (BBA) - Protein Structure and Molecular Enzymology, Vol. 994, Issue 1 https://doi.org/10.1016/0167-4838(89)90062-9	journal	January 1989
Inverse suspension polymerization of acrylamide Dimonie, M. V.; Boghina, C. M.; Marinescu, N. N. European Polymer Journal, Vol. 18, Issue 7 https://doi.org/10.1016/0014-3057(82)90043-X	journal	January 1982
Mass spectrometric characterization of the oxidation of the fluorescent lipid peroxidation reporter molecule C11-BODIPY581/591 Drummen, Gregor P. C.; Gadella, Barend M.; Post, Jan A. Free Radical Biology and Medicine, Vol. 36, Issue 12 https://doi.org/10.1016/j.freeradbiomed.2004.03.014	journal	June 2004
Physical and enzymatic properties of lignin peroxidase isoenzymes from Phanerochaete chrysosporium Farrell, Roberta L.; Murtagh, Karen E.; Tien, Ming Enzyme and Microbial Technology, Vol. 11, Issue 6 https://doi.org/10.1016/0141-0229(89)90014-8	journal	June 1989
Evaluating Isolates of Phanerochaete chrysosporium and Ceriporiopsis subvermispora for Use in Biological Pulping Processes Blanchette, Robert A.; Burnes, Todd A.; Eerdmans, Marjorie M. Holzforschung, Vol. 46, Issue 2 https://doi.org/10.1515/hfsg.1992.46.2.109	journal	January 1992
Evidence for Veratryl Alcohol as a Redox Mediator in Lignin Peroxidase-Catalyzed Oxidation Goodwin, Douglas C.; Aust, Steven D.; Grover, Thomas A. Biochemistry, Vol. 34, Issue 15 https://doi.org/10.1021/bi00015a017	journal	April 1995
Expression of lignin peroxidase H8 in Escherichia coli: folding and activation of the recombinant enzyme with Ca2+ and haem Doyle, Wendy A.; Smith, Andrew T. Biochemical Journal, Vol. 315, Issue 1 https://doi.org/10.1042/bj3150015	journal	April 1996
Aryl alcohols in the physiology of ligninolytic fungi Jong, Ed; Field, Jim A.; Bont, Jan A. M. FEMS Microbiology Reviews, Vol. 13, Issue 2-3 https://doi.org/10.1111/j.1574-6976.1994.tb00041.x	journal	March 1994
The mediation of veratryl alcohol in oxidations promoted by lignin peroxidase: the lifetime of veratryl alcohol radical cation Baciocchi, Enrico; Bietti, Massimo; Francesca Gerini, Maria Biochemical and Biophysical Research Communications, Vol. 293, Issue 2 https://doi.org/10.1016/S0006-291X(02)00306-6	journal	May 2002
Mapping the Long-Range Electron Transfer Route in Ligninolytic Peroxidases Acebes, Sandra; Ruiz-Dueñas, Francisco J.; Toubes, Mario The Journal of Physical Chemistry B, Vol. 121, Issue 16 https://doi.org/10.1021/acs.jpcb.7b00835	journal	April 2017
Effect of Mn(II) on reactions catalyzed by lignin peroxidase from Phanerochaete chrysosporium Bono, Jean-Jacques; Goulas, Philippe; Boe, Jean-Francois European Journal of Biochemistry, Vol. 192, Issue 1 https://doi.org/10.1111/j.1432-1033.1990.tb19213.x	journal	August 1990
Oxidation of 4-Methoxymandelic Acid by Lignin Peroxidase: MEDIATION BY VERATRYL ALCOHOL Tien, Ming; Ma, Dengbo Journal of Biological Chemistry, Vol. 272, Issue 14 https://doi.org/10.1074/jbc.272.14.8912	journal	April 1997
Spatial mapping of extracellular oxidant production by a white rot basidiomycete on wood reveals details of ligninolytic mechanism: Mapping of fungal oxidant production on wood Hunt, Christopher G.; Houtman, Carl J.; Jones, Don C. Environmental Microbiology, Vol. 15, Issue 3 https://doi.org/10.1111/1462-2920.12039	journal	December 2012
Cell wall alterations in loblolly pine wood decayed by the white-rot fungus, Ceriporiopsis subvermispora Blanchette, Robert A.; W. Krueger, Eugene; Haight, John E. Journal of Biotechnology, Vol. 53, Issue 2-3 https://doi.org/10.1016/S0168-1656(97)01674-X	journal	March 1997
Mechanism of oxidative C alpha-C beta cleavage of a lignin model dimer by Phanerochaete chrysosporium ligninase. Stoichiometry and involvement of free radicals. Hammel, K. E.; Tien, M.; Kalyanaraman, B. Journal of Biological Chemistry, Vol. 260, Issue 14 https://doi.org/10.1016/S0021-9258(17)39479-6	journal	July 1985
Evidence that cellobiose oxidase from Phanerochaete chrysosporium is primarily an Fe(III) reductas. Kinetic comparison with neutrophil NADPH oxidase and yeast flavocytochrome b2 Kremer, Simon M.; Wood, Paul M. European Journal of Biochemistry, Vol. 205, Issue 1 https://doi.org/10.1111/j.1432-1033.1992.tb16760.x	journal	April 1992
Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown rot fungi Filley, T. R.; Cody, G. D.; Goodell, B. Organic Geochemistry, Vol. 33, Issue 2 https://doi.org/10.1016/S0146-6380(01)00144-9	journal	February 2002
FiPy: Partial Differential Equations with Python Guyer, Jonathan E.; Wheeler, Daniel; Warren, James A. Computing in Science & Engineering, Vol. 11, Issue 3 https://doi.org/10.1109/MCSE.2009.52	journal	May 2009
Characterization of a Novel Manganese Peroxidase-Lignin Peroxidase Hybrid Isozyme Produced by Bjerkandera Species Strain BOS55 in the Absence of Manganese Mester, Tünde; Field, Jim A. Journal of Biological Chemistry, Vol. 273, Issue 25 https://doi.org/10.1074/jbc.273.25.15412	journal	June 1998
Ligninolysis by a purified lignin peroxidase Hammel, K. E.; Jensen, K. A.; Mozuch, M. D. Journal of Biological Chemistry, Vol. 268, Issue 17 https://doi.org/10.1016/S0021-9258(18)31385-1	journal	June 1993
Derivatization of cross-linked polyacrylamide beads. Controlled introduction of functional groups for the preparation of special-purpose, biochemical adsorbents Inman, John K.; Dintzis, Howard M. Biochemistry, Vol. 8, Issue 10 https://doi.org/10.1021/bi00838a026	journal	October 1969
Evidence for formation of the veratryl alcohol cation radical by lignin peroxidase Khindaria, Aditya; Grover, Thomas A.; Aust, Steven D. Biochemistry, Vol. 34, Issue 18 https://doi.org/10.1021/bi00018a003	journal	May 1995
Kinetics of oxidation of benzyl alcohols by the dication and radical cation of ABTS. Comparison with laccase–ABTS oxidations: an apparent paradox Branchi, Barbara; Galli, Carlo; Gentili, Patrizia Organic & Biomolecular Chemistry, Vol. 3, Issue 14 https://doi.org/10.1039/b504199f	journal	January 2005
A Kinetic Study of the Reaction of Horseradish Peroxidase with Hydrogen Peroxide Dolman, D.; Newell, G. A.; Thurlow, M. D. Canadian Journal of Biochemistry, Vol. 53, Issue 5 https://doi.org/10.1139/o75-069	journal	May 1975
Veratryl alcohol as a mediator and the role of radical cations in lignin biodegradation by Phanerochaete chrysosporium Harvey, P. J.; Schoemaker, H. E.; Palmer, J. M. FEBS Letters, Vol. 195, Issue 1-2 https://doi.org/10.1016/0014-5793(86)80168-5	journal	January 1986
Permeability studies on horse liver alcohol dehydrogenase (HLAD) in polyacrylamide gel beads Gorrebeeck, C.; Lemière, G. L.; Dommisse, R. A. Recueil des Travaux Chimiques des Pays-Bas, Vol. 110, Issue 5 https://doi.org/10.1002/recl.19911100518	journal	January 1991
Demonstration of Lignin-to-Peroxidase Direct Electron Transfer: A TRANSIENT-STATE KINETICS, DIRECTED MUTAGENESIS, EPR, AND NMR STUDY Sáez-Jiménez, Verónica; Baratto, Maria Camilla; Pogni, Rebecca Journal of Biological Chemistry, Vol. 290, Issue 38 https://doi.org/10.1074/jbc.M115.665919	journal	August 2015
The Paleozoic Origin of Enzymatic Lignin Decomposition Reconstructed from 31 Fungal Genomes Floudas, Dimitrios; Binder, Manfred; Riley, Robert Science, Vol. 336, Issue 6089 https://doi.org/10.1126/science.1221748	journal	June 2012
Oxidation of Guaiacol by Lignin Peroxidase: ROLE OF VERATRYL ALCOHOL Koduri, Rao S.; Tien, Ming Journal of Biological Chemistry, Vol. 270, Issue 38 https://doi.org/10.1074/jbc.270.38.22254	journal	September 1995
Stabilization of the Veratryl Alcohol Cation Radical by Lignin Peroxidase ^† Khindaria, Aditya; Yamazaki, Isao; Aust, Steven D. Biochemistry, Vol. 35, Issue 20 https://doi.org/10.1021/bi9601666	journal	January 1996
Comparison of ligninase-I and peroxidase-M2 from the white-rot fungus Phanerochaete chrysosporium Paszczyński, Andrzej; Huynh, Van-Ba; Crawford, Ronald Archives of Biochemistry and Biophysics, Vol. 244, Issue 2, p. 750-765 https://doi.org/10.1016/0003-9861(86)90644-2	journal	February 1986
Description of a Versatile Peroxidase Involved in the Natural Degradation of Lignin That Has Both Manganese Peroxidase and Lignin Peroxidase Substrate Interaction Sites Camarero, Susana; Sarkar, Sovan; Ruiz-Dueñas, Francisco Javier Journal of Biological Chemistry, Vol. 274, Issue 15 https://doi.org/10.1074/jbc.274.15.10324	journal	April 1999
The involvement of hydroxyl radical derived from hydrogen peroxide in lignin degradation by the white rot fungus Phanerochaete chrysosporium. Forney, L. J.; Reddy, C. A.; Tien, M. Journal of Biological Chemistry, Vol. 257, Issue 19 https://doi.org/10.1016/S0021-9258(18)33781-5	journal	October 1982
Do the extracellular enzymes cellobiose dehydrogenase and manganese peroxidase form a pathway in lignin biodegradation? Hildén, Lars; Johansson, Gunnar; Pettersson, Göran FEBS Letters, Vol. 477, Issue 1-2 https://doi.org/10.1016/S0014-5793(00)01757-9	journal	July 2000
Comparative genomics of Ceriporiopsis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis Fernandez-Fueyo, E.; Ruiz-Duenas, F. J.; Ferreira, P. Proceedings of the National Academy of Sciences, Vol. 109, Issue 14, p. 5458-5463 https://doi.org/10.1073/pnas.1119912109	journal	March 2012
Role of fungal peroxidases in biological ligninolysis Hammel, K.; Cullen, D. Current Opinion in Plant Biology, Vol. 11, Issue 3 https://doi.org/10.1016/j.pbi.2008.02.003	journal	June 2008
Molecular biology and structure-function of lignin-degrading heme peroxidases Martı́nez, Angel T. Enzyme and Microbial Technology, Vol. 30, Issue 4 https://doi.org/10.1016/S0141-0229(01)00521-X	journal	April 2002
Kinetic studies on the formation and decomposition of compounds II and III. Reactions of lignin peroxidase with H2O2. Cai, D.; Tien, M. Journal of Biological Chemistry, Vol. 267, Issue 16 https://doi.org/10.1016/S0021-9258(19)49888-8	journal	June 1992
Ligninase of Phanerochaete chrysosporium. Mechanism of its degradation of the non-phenolic arylglycerol β-aryl ether substructure of lignin Kirk, T. K.; Tien, M.; Kersten, P. J. Biochemical Journal, Vol. 236, Issue 1 https://doi.org/10.1042/bj2360279	journal	May 1986
Substrate free radicals are intermediates in ligninase catalysis. Hammel, K. E.; Kalyanaraman, B.; Kirk, T. K. Proceedings of the National Academy of Sciences, Vol. 83, Issue 11 https://doi.org/10.1073/pnas.83.11.3708	journal	June 1986
Veratryl alcohol oxidation by lignin peroxidase Khindaria, Aditya; Yamazaki, Isao; Aust, Steven D. Biochemistry, Vol. 34, Issue 51 https://doi.org/10.1021/bi00051a037	journal	December 1995
Lifetime, Reduction Potential and Base-Induced Fragmentation of the Veratryl Alcohol Radical Cation in Aqueous Solution. Pulse Radiolysis Studies on a Ligninase “Mediator” Bietti, Massimo; Baciocchi, Enrico; Steenken, Steen The Journal of Physical Chemistry A, Vol. 102, Issue 38 https://doi.org/10.1021/jp9812482	journal	September 1998
Lifetime and Reactivity of the Veratryl Alcohol Radical Cation.: IMPLICATIONS FOR LIGNIN PEROXIDASE CATALYSIS Candeias, Luis P.; Harvey, Patricia J. Journal of Biological Chemistry, Vol. 270, Issue 28 https://doi.org/10.1074/jbc.270.28.16745	journal	July 1995
Steady-state and transient-state kinetic studies on the oxidation of 3,4-dimethoxybenzyl alcohol catalyzed by the ligninase of Phanerocheate chrysosporium Burds. Tien, M.; Kirk, T. K.; Bull, C. Journal of Biological Chemistry, Vol. 261, Issue 4 https://doi.org/10.1016/S0021-9258(17)35994-X	journal	February 1986
Diffusion Coefficients of Aromatics in Aqueous Solution Niesner, René; Heintz, Andreas Journal of Chemical & Engineering Data, Vol. 45, Issue 6 https://doi.org/10.1021/je0000569	journal	November 2000
Comparative Genomics of Early-Diverging Mushroom-Forming Fungi Provides Insights into the Origins of Lignocellulose Decay Capabilities Nagy, László G.; Riley, Robert; Tritt, Andrew Molecular Biology and Evolution, Vol. 33, Issue 4 https://doi.org/10.1093/molbev/msv337	journal	December 2015
Role of surface tryptophan for peroxidase oxidation of nonphenolic lignin Sáez-Jiménez, Verónica; Rencoret, Jorge; Rodríguez-Carvajal, Miguel Angel Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0615-x	journal	September 2016
Diffusion coefficients of oxygen, hydrogen peroxide and glucose in a hydrogel van Stroe-Biezen, S. A. M.; Everaerts, F. M.; Janssen, L. J. J. Analytica Chimica Acta, Vol. 273, Issue 1-2 https://doi.org/10.1016/0003-2670(93)80202-V	journal	February 1993
Flash CIDNP Study of Photosensitized Electron Transfer Reactions of Methoxybenzenes Goez, Martin; Eckert, Gerd Berichte der Bunsengesellschaft für physikalische Chemie, Vol. 95, Issue 10 https://doi.org/10.1002/bbpc.19910951004	journal	October 1991
Studying the binding mechanisms of veratryl alcohol to P. chrysosporium lignin peroxidase: insights from theoretical approaches Recabarren, Rodrigo; Fuenzalida-Valdivia, Isabel; Alzate-Morales, Jans Theoretical Chemistry Accounts, Vol. 135, Issue 3 https://doi.org/10.1007/s00214-016-1828-6	journal	March 2016
Regulation of Gene Expression during the Onset of Ligninolytic Oxidation by Phanerochaete chrysosporium on Spruce Wood Korripally, Premsagar; Hunt, Christopher G.; Houtman, Carl J. Applied and Environmental Microbiology, Vol. 81, Issue 22 https://doi.org/10.1128/AEM.02064-15	journal	September 2015
Comparison of lignin peroxidase, horseradish peroxidase and laccase in the oxidation of methoxybenzenes Kersten, P. J.; Kalyanaraman, B.; Hammel, K. E. Biochemical Journal, Vol. 268, Issue 2 https://doi.org/10.1042/bj2680475	journal	June 1990

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59 BASIC BIOLOGICAL SCIENCES
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
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Title: Fungal lignin peroxidase does not produce the veratryl alcohol cation radical as a diffusible ligninolytic oxidant

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