skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Peroxidase versus Peroxygenase Activity: Substrate Substituent Effects as Modulators of Enzyme Function in the Multifunctional Catalytic Globin Dehaloperoxidase

Abstract

The dehaloperoxidase-hemoglobin (DHP) from the terebellid polychaete Amphitrite ornata is a multifunctional hemoprotein that catalyzes the oxidation of a wide variety of substrates, including halo/nitrophenols, haloindoles, and pyrroles, via peroxidase and/or peroxygenase mechanisms. To probe whether substrate substituent effects can modulate enzyme activity in DHP, we investigated its reactiviy against a panel of o-guaiacol substrates given their presence (from native/halogenated and non-native/anthropogenic sources) in the benthic environment that A. ornata inhabits. Using biochemical assays supported by spectroscopic, spectrometric, and structural studies, DHP was found to catalyze the H2O2-dependent oxidative dehalogenation of 4-haloguaiacols (F, Cl, and Br) to 2-methoxybenzoquinone (2-MeOBQ). 18O labeling studies confirmed that O atom incorporation was derived exclusively from water, consistent with substrate oxidation via a peroxidase-based mechanism. Here, the 2-MeOBQ product further reduced DHP to its oxyferrous state, providing a link between the substrate oxidation and O2 carrier functions of DHP. Nonnative substrates resulted in polymerization of the initial substrate with varying degrees of oxidation, with 2-MeOBQ identified as a minor product. When viewed alongside the reactivity of previously studied phenolic substrates, the results presented here show that simple substituent effects can serve as functional switches between peroxidase and peroxygenase activities in this multifunctional catalytic globin. Moremore » broadly, when recent findings on DHP activity with nitrophenols and azoles are included, the results presented here further demonstrate the breadth of heterocyclic compounds of anthropogenic origin that can potentially disrupt marine hemoglobins or function as environmental stressors, findings that may be important when assessing the environmental impact of these pollutants (and their metabolites) on aquatic systems.« less

Authors:
 [1];  [1];  [1];  [1]; ORCiD logo [1]
  1. North Carolina State Univ., Raleigh, NC (United States)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES); National Science Foundation (NSF)
OSTI Identifier:
1467729
Grant/Contract Number:  
W-31-109-Eng-38; CHE-1150709; CHE-1609446; CHE-1659690
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Biochemistry
Additional Journal Information:
Journal Volume: 57; Journal Issue: 30; Journal ID: ISSN 0006-2960
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
ENGLISH
Subject:
59 BASIC BIOLOGICAL SCIENCES; 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; redox reactions; bioinorganic chemistry; peptides and proteins; surface interactions; oxidation; globin; guaiacol; heme; peroxidase; peroxygenase; structure-function

Citation Formats

McGuire, Ashlyn H., Carey, Leiah M., de Serrano, Vesna, Dali, Safaa, and Ghiladi, Reza A. Peroxidase versus Peroxygenase Activity: Substrate Substituent Effects as Modulators of Enzyme Function in the Multifunctional Catalytic Globin Dehaloperoxidase. United States: N. p., 2018. Web. doi:10.1021/acs.biochem.8b00540.
McGuire, Ashlyn H., Carey, Leiah M., de Serrano, Vesna, Dali, Safaa, & Ghiladi, Reza A. Peroxidase versus Peroxygenase Activity: Substrate Substituent Effects as Modulators of Enzyme Function in the Multifunctional Catalytic Globin Dehaloperoxidase. United States. https://doi.org/10.1021/acs.biochem.8b00540
McGuire, Ashlyn H., Carey, Leiah M., de Serrano, Vesna, Dali, Safaa, and Ghiladi, Reza A. 2018. "Peroxidase versus Peroxygenase Activity: Substrate Substituent Effects as Modulators of Enzyme Function in the Multifunctional Catalytic Globin Dehaloperoxidase". United States. https://doi.org/10.1021/acs.biochem.8b00540. https://www.osti.gov/servlets/purl/1467729.
@article{osti_1467729,
title = {Peroxidase versus Peroxygenase Activity: Substrate Substituent Effects as Modulators of Enzyme Function in the Multifunctional Catalytic Globin Dehaloperoxidase},
author = {McGuire, Ashlyn H. and Carey, Leiah M. and de Serrano, Vesna and Dali, Safaa and Ghiladi, Reza A.},
abstractNote = {The dehaloperoxidase-hemoglobin (DHP) from the terebellid polychaete Amphitrite ornata is a multifunctional hemoprotein that catalyzes the oxidation of a wide variety of substrates, including halo/nitrophenols, haloindoles, and pyrroles, via peroxidase and/or peroxygenase mechanisms. To probe whether substrate substituent effects can modulate enzyme activity in DHP, we investigated its reactiviy against a panel of o-guaiacol substrates given their presence (from native/halogenated and non-native/anthropogenic sources) in the benthic environment that A. ornata inhabits. Using biochemical assays supported by spectroscopic, spectrometric, and structural studies, DHP was found to catalyze the H2O2-dependent oxidative dehalogenation of 4-haloguaiacols (F, Cl, and Br) to 2-methoxybenzoquinone (2-MeOBQ). 18O labeling studies confirmed that O atom incorporation was derived exclusively from water, consistent with substrate oxidation via a peroxidase-based mechanism. Here, the 2-MeOBQ product further reduced DHP to its oxyferrous state, providing a link between the substrate oxidation and O2 carrier functions of DHP. Nonnative substrates resulted in polymerization of the initial substrate with varying degrees of oxidation, with 2-MeOBQ identified as a minor product. When viewed alongside the reactivity of previously studied phenolic substrates, the results presented here show that simple substituent effects can serve as functional switches between peroxidase and peroxygenase activities in this multifunctional catalytic globin. More broadly, when recent findings on DHP activity with nitrophenols and azoles are included, the results presented here further demonstrate the breadth of heterocyclic compounds of anthropogenic origin that can potentially disrupt marine hemoglobins or function as environmental stressors, findings that may be important when assessing the environmental impact of these pollutants (and their metabolites) on aquatic systems.},
doi = {10.1021/acs.biochem.8b00540},
url = {https://www.osti.gov/biblio/1467729}, journal = {Biochemistry},
issn = {0006-2960},
number = 30,
volume = 57,
place = {United States},
year = {Wed Jun 27 00:00:00 EDT 2018},
month = {Wed Jun 27 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 17 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Treatment of pulp and paper mill wastewater—a review
journal, October 2004


Degradation of 4-Chloroguaiacol by Dark Fenton and Solar Photo-Fenton Advanced Oxidation Processes
journal, December 2009


Kinetic degradation of the pollutant guaiacol by dark Fenton and solar photo-Fenton processes
journal, May 2011


Unraveling Pathways of Guaiacol Nitration in Atmospheric Waters: Nitrite, A Source of Reactive Nitronium Ion in the Atmosphere
journal, July 2015


Biosynthesis of polybrominated aromatic organic compounds by marine bacteria
journal, June 2014


Solubility and Infinite Dilution Activity Coefficient for 5-Chlorovanillin and 4-Chloroguaiacol in Water over the Temperature Range 280 to 363 K
journal, March 2000


Does toxicity of aromatic pollutants increase under remote atmospheric conditions?
journal, March 2015


Acute toxicity of emerging atmospheric pollutants from wood lignin due to biomass burning
journal, September 2017


Oxidation of Guaiacol by Lignin Peroxidase: ROLE OF VERATRYL ALCOHOL
journal, September 1995


Engineered Bacillus pumilus laccase-like multi-copper oxidase for enhanced oxidation of the lignin model compound guaiacol
journal, May 2017


Structural and spectroscopic characterisation of a heme peroxidase from sorghum
journal, December 2015


Influence of temperature, pH and metal ions on guaiacol oxidation of purified laccase from Leptographium qinlingensis
journal, November 2013


An enzymatic globin from a marine worm
journal, September 1999


The dehaloperoxidase paradox
journal, April 2012


Hemoglobins of two terebellid polychaetes: Enoplobranchus sanguineus and Amphitrite ornata
journal, January 1977


The Crystal Structure and Amino Acid Sequence of Dehaloperoxidase from Amphitrite ornata Indicate Common Ancestry with Globins
journal, June 2000


Peroxygenase and Oxidase Activities of Dehaloperoxidase-Hemoglobin from Amphitrite ornata
journal, May 2014


Oxidation of pyrrole by dehaloperoxidase-hemoglobin: chemoenzymatic synthesis of pyrrolin-2-ones
journal, January 2017


How nature tunes isoenzyme activity in the multifunctional catalytic globin dehaloperoxidase from Amphitrite ornata
journal, February 2018


Selective tuning of activity in a multifunctional enzyme as revealed in the F21W mutant of dehaloperoxidase B from Amphitrite ornata
journal, November 2017


Tyrosyl Radicals in Dehaloperoxidase
journal, November 2013


Compound ES of Dehaloperoxidase Decays via Two Alternative Pathways Depending on the Conformation of the Distal Histidine
journal, December 2010


Characterization of Dehaloperoxidase Compound ES and Its Reactivity with Trihalophenols
journal, February 2009


Nonmicrobial Nitrophenol Degradation via Peroxygenase Activity of Dehaloperoxidase-Hemoglobin from Amphitrite ornata
journal, April 2016


Amphitrite ornata, a Marine Worm, Contains Two Dehaloperoxidase Genes
journal, May 2001


Structure of dehaloperoxidase B at 1.58 Å resolution and structural characterization of the AB dimer from Amphitrite ornata
journal, April 2010


Probing the Oxyferrous and Catalytically Active Ferryl States of Amphitrite ornata Dehaloperoxidase by Cryoreduction and EPR/ENDOR Spectroscopy. Detection of Compound I
journal, October 2010


Spectroscopic and Mechanistic Investigations of Dehaloperoxidase B from Amphitrite ornata
journal, August 2010


Kinetic Study of the Inhibition Mechanism of Dehaloperoxidase-Hemoglobin A by 4-Bromophenol
journal, July 2013


The natural production of organobromine compounds
journal, March 2000


Role of tryptophan-208 residue in cytochrome c oxidation by ascorbate peroxidase from Leishmania major-kinetic studies on Trp208Phe mutant and wild type enzyme
journal, May 2008


Immobilization of myoglobin from horse skeletal muscle in hydrophilic polymer networks
journal, January 2007


Measuring Binding Affinity of Protein−Ligand Interaction Using Spectrophotometry: Binding of Neutral Red to Riboflavin-Binding Protein
journal, June 2010


Phaser crystallographic software
journal, July 2007


PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010


The CCP4 suite programs for protein crystallography
journal, September 1994


Features and development of Coot
journal, March 2010


Refinement of Macromolecular Structures by the Maximum-Likelihood Method
journal, May 1997


Towards automated crystallographic structure refinement with phenix.refine
journal, March 2012


An Unusual Dehalogenating Peroxidase from the Marine Terebellid Polychaete Amphitrite ornata
journal, March 1996


Internal Binding of Halogenated Phenols in Dehaloperoxidase-Hemoglobin Inhibits Peroxidase Function
journal, September 2010


Guaiacol Oxidation Products in the Enzyme-Activity Assay Reaction by Horseradish Peroxidase Catalysis
journal, July 2004


Identification of the Colored Guaiacol Oxidation Product Produced by Peroxidases
journal, July 1997


Oxidative Coupling and Polymerization of Guaiacol, a Lignin Derivative
journal, September 1988


An unexpected side reaction in the guaiacol assay for peroxidase
journal, September 1992


Hybridization of Modified-Heme Reconstitution and Distal Histidine Mutation to Functionalize Sperm Whale Myoglobin
journal, January 2004


Peroxidase Activity of Myoglobin Is Enhanced by Chemical Mutation of Heme-Propionates
journal, September 1999


Lignin and Mn Peroxidase-Catalyzed Oxidation of Phenolic Lignin Oligomers
journal, March 1999


Dehydrogenation of Phenols. II. Dehydrogenation Polymers from Guaiacol.
journal, January 1960


The reaction of guaiacol with iron III and chromium VI compounds as a model for wood surface modification
journal, June 1995


Dehydrogenation of Phenols. I. Dehydrogenation of 2,6-Dimethylphenol with Silver Oxide.
journal, January 1960


Applications of Absorption Spectroelectrochemistry in Artificial Blood Research
journal, December 2004


Optically transparent thin layer electrode techniquesfor the study of biological redox systems
journal, January 1979


Redox reactivity of the heme Fe3+/Fe2+ couple in native myoglobins and mutants with peroxidase-like activity
journal, June 2007


Redox Thermodynamics of the Fe(III)/Fe(II) Couple of Human Myeloperoxidase in Its High-Spin and Low-Spin Forms
journal, October 2006


Nonphotochemical Base-Catalyzed Hydroxylation of 2,6-Dichloroquinone by H 2 O 2 Occurs by a Radical Mechanism
journal, January 2012


On the function and mechanism of action of peroxidases
journal, August 1976


Works referencing / citing this record: