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Article

Agaricales Mushroom Lignin Peroxidase: From Structure–Function to Degradative Capabilities

1
Centro de Investigaciones Biológicas “Margarita Salas” (CIB), Consejo Superior de Investigaciones Científicas (CSIC), 28040 Madrid, Spain
2
Instituto de Recursos Naturales y Agrobiología de Sevilla (IRNAS), Consejo Superior de Investigaciones Científicas (CSIC), 41012 Seville, Spain
*
Authors to whom correspondence should be addressed.
These two authors contributed equally to this work.
Current address: Norwegian University of Life Sciences (NMBU), 1430 Ås, Norway.
§
Current address: Institute for Biocomputation and Physics of Complex Systems, 50013 Zaragoza, Spain.
Academic Editor: Marcel Zamocky
Antioxidants 2021, 10(9), 1446; https://doi.org/10.3390/antiox10091446
Received: 18 August 2021 / Revised: 7 September 2021 / Accepted: 8 September 2021 / Published: 12 September 2021
Lignin biodegradation has been extensively studied in white-rot fungi, which largely belong to order Polyporales. Among the enzymes that wood-rotting polypores secrete, lignin peroxidases (LiPs) have been labeled as the most efficient. Here, we characterize a similar enzyme (ApeLiP) from a fungus of the order Agaricales (with ~13,000 described species), the soil-inhabiting mushroom Agrocybe pediades. X-ray crystallography revealed that ApeLiP is structurally related to Polyporales LiPs, with a conserved heme-pocket and a solvent-exposed tryptophan. Its biochemical characterization shows that ApeLiP can oxidize both phenolic and non-phenolic lignin model-compounds, as well as different dyes. Moreover, using stopped-flow rapid spectrophotometry and 2D-NMR, we demonstrate that ApeLiP can also act on real lignin. Characterization of a variant lacking the above tryptophan residue shows that this is the oxidation site for lignin and other high redox-potential substrates, and also plays a role in phenolic substrate oxidation. The reduction potentials of the catalytic-cycle intermediates were estimated by stopped-flow in equilibrium reactions, showing similar activation by H2O2, but a lower potential for the rate-limiting step (compound-II reduction) compared to other LiPs. Unexpectedly, ApeLiP was stable from acidic to basic pH, a relevant feature for application considering its different optima for oxidation of phenolic and nonphenolic compounds. View Full-Text
Keywords: Agaricales; lignin peroxidase; catalytic tryptophan; crystal structure; transient-state kinetics; reduction potential; model dimers; non-phenolic lignin; lignosulfonate degradation; NMR spectroscopy Agaricales; lignin peroxidase; catalytic tryptophan; crystal structure; transient-state kinetics; reduction potential; model dimers; non-phenolic lignin; lignosulfonate degradation; NMR spectroscopy
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MDPI and ACS Style

Sánchez-Ruiz, M.I.; Ayuso-Fernández, I.; Rencoret, J.; González-Ramírez, A.M.; Linde, D.; Davó-Siguero, I.; Romero, A.; Gutiérrez, A.; Martínez, A.T.; Ruiz-Dueñas, F.J. Agaricales Mushroom Lignin Peroxidase: From Structure–Function to Degradative Capabilities. Antioxidants 2021, 10, 1446. https://doi.org/10.3390/antiox10091446

AMA Style

Sánchez-Ruiz MI, Ayuso-Fernández I, Rencoret J, González-Ramírez AM, Linde D, Davó-Siguero I, Romero A, Gutiérrez A, Martínez AT, Ruiz-Dueñas FJ. Agaricales Mushroom Lignin Peroxidase: From Structure–Function to Degradative Capabilities. Antioxidants. 2021; 10(9):1446. https://doi.org/10.3390/antiox10091446

Chicago/Turabian Style

Sánchez-Ruiz, María I., Iván Ayuso-Fernández, Jorge Rencoret, Andrés M. González-Ramírez, Dolores Linde, Irene Davó-Siguero, Antonio Romero, Ana Gutiérrez, Angel T. Martínez, and Francisco J. Ruiz-Dueñas. 2021. "Agaricales Mushroom Lignin Peroxidase: From Structure–Function to Degradative Capabilities" Antioxidants 10, no. 9: 1446. https://doi.org/10.3390/antiox10091446

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