Mechanistic Insights into Dye-Decolorizing Peroxidase Revealed by Solvent Isotope and Viscosity Effects

Shrestha, Ruben; Huang, Gaochao; Meekins, David A.; Geisbrecht, Brian V.; Li, Ping

doi:10.1021/acscatal.7b01861

Title: Mechanistic Insights into Dye-Decolorizing Peroxidase Revealed by Solvent Isotope and Viscosity Effects

Journal Article · Wed Aug 09 00:00:00 EDT 2017 · ACS Catalysis

DOI:https://doi.org/10.1021/acscatal.7b01861· OSTI ID:1408114

Shrestha, Ruben ^[1]; Huang, Gaochao ^[1]; Meekins, David A. ^[1]; Geisbrecht, Brian V. ^[2];

^[1]

Kansas State Univ., Manhattan, KS (United States). Dept. of Chemistry
Kansas State Univ., Manhattan, KS (United States). Dept. of Biochemistry and Molecular Biophysics

Dye-decolorizing peroxidases (DyPs) are a family of H₂O₂-dependent heme peroxidases that have shown potential applications in lignin degradation and valorization. However, the DyP kinetic mechanism remains underexplored. Using structural biology and solvent isotope (sKIE) and viscosity effects, many mechanistic characteristics have been determined for the B-class ElDyP from Enterobacter lignolyticus. Its structure revealed that a water molecule acts as the sixth axial ligand and two channels at diameters of ~3.0 and 8.0 Å lead to the heme center. A conformational change of ERS* to ERS, which have identical spectral characteristics, was proposed as the final step in DyPs’ bisubstrate Ping-Pong mechanism. This step is also the rate-determining step in ABTS oxidation. The normal KIE of wild-type ElDyP with D₂O₂ at pD 3.5 suggested that compound 0 deprotonation by the distal aspartate is rate-limiting in the formation of compound I, which is more reactive under acidic pH than under neutral or alkaline pH. The viscosity effects and other biochemical methods implied that the reducing substrate binds with compound I instead of the free enzyme. The significant inverse sKIEs of k_cat/K_M and k_ERS* suggested that the aquo release in ElDyP is mechanistically important and may explain the enzyme’s adoption of two-electron reduction for compound I. The distal aspartate is catalytically more important than the distal arginine and plays key roles in determining ElDyP’s optimum acidic pH. The kinetic mechanism of D143H-ElDyP was also briefly studied. The results obtained will pave the way for future protein engineering to improve DyPs’ lignolytic activity.

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Research Organization:: Argonne National Lab. (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE

OSTI ID:: 1408114

Journal Information:: ACS Catalysis, Vol. 7, Issue 9; ISSN 2155-5435

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: ENGLISH

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Cited by: 42 works

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References (61)

The multihued palette of dye-decolorizing peroxidases Singh, Rahul; Eltis, Lindsay D. Archives of Biochemistry and Biophysics, Vol. 574 https://doi.org/10.1016/j.abb.2015.01.014	journal	May 2015
DyP-type peroxidases comprise a novel heme peroxidase family Sugano, Y. Cellular and Molecular Life Sciences, Vol. 66, Issue 8 https://doi.org/10.1007/s00018-008-8651-8	journal	December 2008
Exploring bacterial lignin degradation Brown, Margaret E.; Chang, Michelle CY Current Opinion in Chemical Biology, Vol. 19 https://doi.org/10.1016/j.cbpa.2013.11.015	journal	April 2014
Bacterial enzymes involved in lignin degradation de Gonzalo, Gonzalo; Colpa, Dana I.; Habib, Mohamed H. M. Journal of Biotechnology, Vol. 236 https://doi.org/10.1016/j.jbiotec.2016.08.011	journal	October 2016
The emerging role for bacteria in lignin degradation and bio-product formation Bugg, Timothy DH; Ahmad, Mark; Hardiman, Elizabeth M. Current Opinion in Biotechnology, Vol. 22, Issue 3 https://doi.org/10.1016/j.copbio.2010.10.009	journal	June 2011
Lignin valorization through integrated biological funneling and chemical catalysis Linger, J. G.; Vardon, D. R.; Guarnieri, M. T. Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018 https://doi.org/10.1073/pnas.1410657111	journal	August 2014
Lignocellulose: A chewy problem Sanderson, Katharine Nature, Vol. 474, Issue 7352, p. S12-S14 https://doi.org/10.1038/474S012a	journal	June 2011
The Catalytic Valorization of Lignin for the Production of Renewable Chemicals Zakzeski, Joseph; Bruijnincx, Pieter C. A.; Jongerius, Anna L. Chemical Reviews, Vol. 110, Issue 6, p. 3552-3599 https://doi.org/10.1021/cr900354u	journal	June 2010
Lignin Valorization: Improving Lignin Processing in the Biorefinery Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J. Science, Vol. 344, Issue 6185, p. 1246843-1246843 https://doi.org/10.1126/science.1246843	journal	May 2014
Formic-acid-induced depolymerization of oxidized lignin to aromatics Rahimi, Alireza; Ulbrich, Arne; Coon, Joshua J. Nature, Vol. 515, Issue 7526, p. 249-252 https://doi.org/10.1038/nature13867	journal	November 2014
Lignin Biosynthesis Boerjan, Wout; Ralph, John; Baucher, Marie Annual Review of Plant Biology, Vol. 54, Issue 1, p. 519-546 https://doi.org/10.1146/annurev.arplant.54.031902.134938	journal	June 2003
Characterization of Fermentation Residues from the Production of Bio-Ethanol from Lignocellulosic Feedstocks Sannigrahi, Poulomi; Ragauskas, Arthur J. Journal of Biobased Materials and Bioenergy, Vol. 5, Issue 4 https://doi.org/10.1166/jbmb.2011.1170	journal	December 2011
Structure and Action Mechanism of Ligninolytic Enzymes Wong, Dominic W. S. Applied Biochemistry and Biotechnology, Vol. 157, Issue 2 https://doi.org/10.1007/s12010-008-8279-z	journal	June 2008
Lignin-degrading enzymes Pollegioni, Loredano; Tonin, Fabio; Rosini, Elena FEBS Journal, Vol. 282, Issue 7 https://doi.org/10.1111/febs.13224	journal	February 2015
Pathways for degradation of lignin in bacteria and fungi Bugg, Timothy D. H.; Ahmad, Mark; Hardiman, Elizabeth M. Natural Product Reports, Vol. 28, Issue 12, p. 1883-1896 https://doi.org/10.1039/c1np00042j	journal	January 2011
Identification of DypB from Rhodococcus jostii RHA1 as a Lignin Peroxidase Ahmad, Mark; Roberts, Joseph N.; Hardiman, Elizabeth M. Biochemistry, Vol. 50, Issue 23 https://doi.org/10.1021/bi101892z	journal	June 2011
Identification and Characterization of a Multifunctional Dye Peroxidase from a Lignin-Reactive Bacterium Brown, Margaret E.; Barros, Tiago; Chang, Michelle C. Y. ACS Chemical Biology, Vol. 7, Issue 12 https://doi.org/10.1021/cb300383y	journal	September 2012
Characterization of Dye-decolorizing Peroxidase (DyP) from Thermomonospora curvata Reveals Unique Catalytic Properties of A-type DyPs Chen, Chao; Shrestha, Ruben; Jia, Kaimin Journal of Biological Chemistry, Vol. 290, Issue 38 https://doi.org/10.1074/jbc.M115.658807	journal	July 2015
A dye-decolorizing peroxidase from Bacillus subtilis exhibiting substrate-dependent optimum temperature for dyes and β-ether lignin dimer Min, Kyoungseon; Gong, Gyeongtaek; Woo, Han Min Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep08245	journal	February 2015
Enantioselective Synthesis of Dilignol Model Compounds and Their Stereodiscrimination Study with a Dye-Decolorizing Peroxidase Huang, Gaochao; Shrestha, Ruben; Jia, Kaimin Organic Letters, Vol. 19, Issue 7 https://doi.org/10.1021/acs.orglett.7b00587	journal	March 2017
A structural and functional perspective of DyP-type peroxidase family Yoshida, Toru; Sugano, Yasushi Archives of Biochemistry and Biophysics, Vol. 574 https://doi.org/10.1016/j.abb.2015.01.022	journal	May 2015
DyP-type peroxidases: a promising and versatile class of enzymes Colpa, Dana I.; Fraaije, Marco W.; van Bloois, Edwin Journal of Industrial Microbiology & Biotechnology, Vol. 41, Issue 1 https://doi.org/10.1007/s10295-013-1371-6	journal	November 2013
Complete genome sequence of “Enterobacter lignolyticus” SCF1 DeAngelis, Kristen M.; D’Haeseleer, Patrik; Chivian, Dylan Standards in Genomic Sciences, Vol. 5, Issue 1 https://doi.org/10.4056/sigs.2104875	journal	September 2011
The Escherichia coli Protein YfeX Functions as a Porphyrinogen Oxidase, Not a Heme Dechelatase Dailey, Harry A.; Septer, Alecia N.; Daugherty, Lauren mBio, Vol. 2, Issue 6 https://doi.org/10.1128/mBio.00248-11	journal	November 2011
Bacteria capture iron from heme by keeping tetrapyrrol skeleton intact Létoffé, Sylvie; Heuck, Gesine; Delepelaire, Philippe Proceedings of the National Academy of Sciences, Vol. 106, Issue 28 https://doi.org/10.1073/pnas.0903842106	journal	June 2009
Measurement of protein using bicinchoninic acid Smith, P. K.; Krohn, R. I.; Hermanson, G. T. Analytical Biochemistry, Vol. 150, Issue 1 https://doi.org/10.1016/0003-2697(85)90442-7	journal	October 1985
Simultaneous determination of hemes a, b, and c from pyridine hemochrome spectra Berry, Edward A.; Trumpower, Bernard L. Analytical Biochemistry, Vol. 161, Issue 1 https://doi.org/10.1016/0003-2697(87)90643-9	journal	February 1987
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Characterization of Axial and Proximal Histidine Mutations of the Decaheme Cytochrome MtrA from Shewanella sp. Strain ANA-3 and Implications for the Electron Transport System Reyes, Carolina; Qian, Fang; Zhang, Alissa Journal of Bacteriology, Vol. 194, Issue 21 https://doi.org/10.1128/JB.00890-12	journal	November 2012
Heme Oxygenase His25Ala Mutant: Replacement of the Proximal Histidine Iron Ligand by Exogenous Bases Restores Catalytic Activity Wilks, Angela; Sun, Jie; Loehr, Thomas M. Journal of the American Chemical Society, Vol. 117, Issue 10 https://doi.org/10.1021/ja00115a027	journal	March 1995
Characterization of Dye-Decolorizing Peroxidases from Rhodococcus jostii RHA1 Roberts, Joseph N.; Singh, Rahul; Grigg, Jason C. Biochemistry, Vol. 50, Issue 23 https://doi.org/10.1021/bi200427h	journal	June 2011
A Dye-Decolorizing Peroxidase from Vibrio cholerae Uchida, Takeshi; Sasaki, Miho; Tanaka, Yoshikazu Biochemistry, Vol. 54, Issue 43 https://doi.org/10.1021/acs.biochem.5b00952	journal	October 2015
Crystal structure and biochemical features of dye-decolorizing peroxidase YfeX from Escherichia coli O157 Asp 143 and Arg 232 play divergent roles toward different substrates Liu, Xiuhua; Yuan, Zenglin; Wang, Jiaxu Biochemical and Biophysical Research Communications, Vol. 484, Issue 1 https://doi.org/10.1016/j.bbrc.2017.01.081	journal	February 2017
Crystal structures of pristine and oxidatively processed lignin peroxidase expressed in Escherichia coli and of the W171F variant that eliminates the redox active tryptophan 171. Implications for the reaction mechanism Blodig, Wolfgang; Smith, Andrew T.; Doyle, Wendy A. Journal of Molecular Biology, Vol. 305, Issue 4 https://doi.org/10.1006/jmbi.2000.4346	journal	January 2001
Ultrahigh (0.93Å) resolution structure of manganese peroxidase from Phanerochaete chrysosporium: Implications for the catalytic mechanism Sundaramoorthy, Munirathinam; Gold, Michael H.; Poulos, Thomas L. Journal of Inorganic Biochemistry, Vol. 104, Issue 6 https://doi.org/10.1016/j.jinorgbio.2010.02.011	journal	June 2010
Unveiling the basis of alkaline stability of an evolved versatile peroxidase Sáez-Jiménez, Verónica; Acebes, Sandra; Garcia-Ruiz, Eva Biochemical Journal, Vol. 473, Issue 13 https://doi.org/10.1042/BCJ20160248	journal	June 2016
Heme Enzyme Structure and Function Poulos, Thomas L. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr400415k	journal	January 2014
Oxidative Mechanisms Involved in Lignin Degradation by White-Rot Fungi ten Have, Rimko; Teunissen, Pauline J. M. Chemical Reviews, Vol. 101, Issue 11 https://doi.org/10.1021/cr000115l	journal	November 2001
A robust and extracellular heme-containing peroxidase from Thermobifida fusca as prototype of a bacterial peroxidase superfamily van Bloois, Edwin; Torres Pazmiño, Daniel E.; Winter, Remko T. Applied Microbiology and Biotechnology, Vol. 86, Issue 5 https://doi.org/10.1007/s00253-009-2369-x	journal	December 2009
Protein Ionizable Groups: p K Values and Their Contribution to Protein Stability and Solubility Pace, C. Nick; Grimsley, Gerald R.; Scholtz, J. Martin Journal of Biological Chemistry, Vol. 284, Issue 20 https://doi.org/10.1074/jbc.R800080200	journal	January 2009
Crystal structure of the pristine peroxidase ferryl center and its relevance to proton-coupled electron transfer Chreifi, Georges; Baxter, Elizabeth L.; Doukov, Tzanko Proceedings of the National Academy of Sciences, Vol. 113, Issue 5 https://doi.org/10.1073/pnas.1521664113	journal	January 2016
Mechanism of the Reaction Catalyzed by Acetoacetate Decarboxylase. Importance of Lysine 116 in Determining the p K _a of Active-Site Lysine 115 ^† Highbarger, Lane A.; Gerlt, John A.; Kenyon, George L. Biochemistry, Vol. 35, Issue 1 https://doi.org/10.1021/bi9518306	journal	January 1996
Horseradish peroxidase. XXIX. Reactions in water and deuterium oxide: cyanide binding, compound I formation, and reactions of compounds I and II with ferrocyanide Dunford, H. Brian; Hewson, W. Donald; Steiner, Håkan Canadian Journal of Chemistry, Vol. 56, Issue 22 https://doi.org/10.1139/v78-468	journal	November 1978
Determination of Rate Constants for Rapid Peroxidase Reactions Goodwin, Douglas C.; Yamazaki, Isao; Aust, Steven D. Analytical Biochemistry, Vol. 231, Issue 2 https://doi.org/10.1006/abio.1995.0059	journal	November 1995
Catalytic surface radical in dye-decolorizing peroxidase: a computational, spectroscopic and site-directed mutagenesis study Linde, Dolores; Pogni, Rebecca; Cañellas, Marina Biochemical Journal, Vol. 466, Issue 2 https://doi.org/10.1042/BJ20141211	journal	February 2015
Identification of Surface-Exposed Protein Radicals and A Substrate Oxidation Site in A-Class Dye-Decolorizing Peroxidase from Thermomonospora curvata Shrestha, Ruben; Chen, Xuejie; Ramyar, Kasra X. ACS Catalysis, Vol. 6, Issue 12 https://doi.org/10.1021/acscatal.6b01952	journal	October 2016
The toolbox of Auricularia auricula-judae dye-decolorizing peroxidase – Identification of three new potential substrate-interaction sites Strittmatter, Eric; Serrer, Kerstin; Liers, Christiane Archives of Biochemistry and Biophysics, Vol. 574 https://doi.org/10.1016/j.abb.2014.12.016	journal	May 2015
Crystal structures of dye-decolorizing peroxidase with ascorbic acid and 2,6-dimethoxyphenol Yoshida, Toru; Tsuge, Hideaki; Hisabori, Toru FEBS Letters, Vol. 586, Issue 24 https://doi.org/10.1016/j.febslet.2012.10.049	journal	November 2012
A formula for correlating p K a values determined in D 2 O and H 2 O Krȩżel, Artur; Bal, Wojciech Journal of Inorganic Biochemistry, Vol. 98, Issue 1 https://doi.org/10.1016/j.jinorgbio.2003.10.001	journal	January 2004
The Poulos−Kraut Mechanism of Compound I Formation in Horseradish Peroxidase: A QM/MM Study Derat, Etienne; Shaik, Sason The Journal of Physical Chemistry B, Vol. 110, Issue 21 https://doi.org/10.1021/jp055412e	journal	June 2006
Inverse Solvent Isotope Effects in the NAD-Malic Enzyme Reaction Are the Result of the Viscosity Difference between D2O and H2O: Implications for Solvent Isotope Effect Studies Karsten, William E.; Lai, Chung-Jeng; Cook, Paul F. Journal of the American Chemical Society, Vol. 117, Issue 22 https://doi.org/10.1021/ja00127a002	journal	June 1995
Inverse Solvent Isotope Effects Arising from Substrate Triggering in the Factor Inhibiting Hypoxia Inducible Factor Hangasky, John A.; Saban, Evren; Knapp, Michael J. Biochemistry, Vol. 52, Issue 9 https://doi.org/10.1021/bi3015482	journal	February 2013
A Flexible Glutamine Regulates the Catalytic Activity of Toluene o -Xylene Monooxygenase Liang, Alexandria Deliz; Wrobel, Alexandra T.; Lippard, Stephen J. Biochemistry, Vol. 53, Issue 22 https://doi.org/10.1021/bi500387y	journal	May 2014
Inverse Solvent Isotope Effects Demonstrate Slow Aquo Release from Hypoxia Inducible Factor-Prolyl Hydroxylase (PHD2) Flagg, Shannon C.; Giri, Nitai; Pektas, Serap Biochemistry, Vol. 51, Issue 33 https://doi.org/10.1021/bi300229y	journal	August 2012
Isotope effect studies of chicken liver NADP malic enzyme: role of the metal ion and viscosity dependence Grissom, Charles B.; Cleland, W. W. Biochemistry, Vol. 27, Issue 8 https://doi.org/10.1021/bi00408a039	journal	April 1988
Dissection of the Stepwise Mechanism to β-Lactam Formation and Elucidation of a Rate-determining Conformational Change in β-Lactam Synthetase Raber, Mary L.; Freeman, Michael F.; Townsend, Craig A. Journal of Biological Chemistry, Vol. 284, Issue 1 https://doi.org/10.1074/jbc.M805390200	journal	January 2009
Deuterium isotope effect on the intramolecular electron transfer in Pseudomonas aeruginosa azurin Farver, O.; Zhang, J.; Chi, Q. Proceedings of the National Academy of Sciences, Vol. 98, Issue 8 https://doi.org/10.1073/pnas.071043798	journal	April 2001
Roles of Water in Heme Peroxidase and Catalase Mechanisms Jones, Peter Journal of Biological Chemistry, Vol. 276, Issue 17 https://doi.org/10.1074/jbc.M011413200	journal	January 2001
The steady-state kinetics of peroxidase with 2,2′-azino-di-(3-ethyl-benzthiazoline-6-sulphonic acid) as chromogen Childs, R. E.; Bardsley, W. G. Biochemical Journal, Vol. 145, Issue 1 https://doi.org/10.1042/bj1450093	journal	January 1975
Kinetic evidence for the formation of a Michaelis–Menten-like complex between horseradish peroxidase compound II and di-(N-acetyl-l-tyrosine) Wang, Weichi; NoËL, Stéphanie; Desmadril, Michel Biochemical Journal, Vol. 340, Issue 1 https://doi.org/10.1042/bj3400329	journal	May 1999

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