skip to main content

DOE PAGESDOE PAGES

Title: Structure and mechanism of NOV1, a resveratrol-cleaving dioxygenase

Stilbenes are diphenyl ethene compounds produced naturally in a wide variety of plant species and some bacteria. Stilbenes are also derived from lignin during kraft pulping. Stilbene cleavage oxygenases (SCOs) cleave the central double bond of stilbenes, forming two phenolic aldehydes. Here in this paper, we report the structure of an SCO. The X-ray structure of NOV1 from Novosphingobium aromaticivorans was determined in complex with its substrate resveratrol (1.89 Å), its product vanillin (1.75 Å), and without any bound ligand (1.61 Å). The enzyme is a seven-bladed β-propeller with an iron cofactor coordinated by four histidines. In all three structures, dioxygen is observed bound to the iron in a side-on fashion. These structures, along with EPR analysis, allow us to propose a mechanism in which a ferric-superoxide reactswith substrate activated by deprotonation of a phenol group at position 4 of the substrate, which allows movement of electron density toward the central double bond and thus facilitates reaction with the ferric superoxide electrophile. Correspondingly, NOV1 cleaves a wide range of other stilbene-like compounds with a 4'-OH group, offering potential in processing some solubilized fragments of lignin into monomer aromatic compounds.
Authors:
 [1] ;  [2] ;  [3] ;  [4] ;  [1] ;  [4] ;  [4] ;  [3] ;  [5] ;  [6]
  1. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics & Integrated Bioimaging Division
  2. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics & Integrated Bioimaging Division; Univ. of Louisville, KY (United States). Dept. of Chemical Engineering; Univ. of Louisville, KY (United States). Conn Center for Renewable Energy Research
  3. Univ. of Wisconsin, Madison, WI (United States). College of Agricultural and Life Sciences, Dept. of Biochemistry; Univ. of Wisconsin, Madison, WI (United States). Great Lakes Bioenergy Research Center
  4. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States). Biological and Engineering Sciences Center
  5. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems & Engineering Division
  6. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Molecular Biophysics & Integrated Bioimaging Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering
Publication Date:
Grant/Contract Number:
AC02-05CH11231; FG02-07ER64495
Type:
Published Article
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 113; Journal Issue: 50; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Science Foundation (NSF); National Institutes of Health (NIH)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; stilbene; dioxygenase; structure; carotenoid
OSTI Identifier:
1334195
Alternate Identifier(s):
OSTI ID: 1379612

McAndrew, Ryan P., Sathitsuksanoh, Noppadon, Mbughuni, Michael M., Heins, Richard A., Pereira, Jose H., George, Anthe, Sale, Kenneth L., Fox, Brian G., Simmons, Blake A., and Adams, Paul D.. Structure and mechanism of NOV1, a resveratrol-cleaving dioxygenase. United States: N. p., Web. doi:10.1073/pnas.1608917113.
McAndrew, Ryan P., Sathitsuksanoh, Noppadon, Mbughuni, Michael M., Heins, Richard A., Pereira, Jose H., George, Anthe, Sale, Kenneth L., Fox, Brian G., Simmons, Blake A., & Adams, Paul D.. Structure and mechanism of NOV1, a resveratrol-cleaving dioxygenase. United States. doi:10.1073/pnas.1608917113.
McAndrew, Ryan P., Sathitsuksanoh, Noppadon, Mbughuni, Michael M., Heins, Richard A., Pereira, Jose H., George, Anthe, Sale, Kenneth L., Fox, Brian G., Simmons, Blake A., and Adams, Paul D.. 2016. "Structure and mechanism of NOV1, a resveratrol-cleaving dioxygenase". United States. doi:10.1073/pnas.1608917113.
@article{osti_1334195,
title = {Structure and mechanism of NOV1, a resveratrol-cleaving dioxygenase},
author = {McAndrew, Ryan P. and Sathitsuksanoh, Noppadon and Mbughuni, Michael M. and Heins, Richard A. and Pereira, Jose H. and George, Anthe and Sale, Kenneth L. and Fox, Brian G. and Simmons, Blake A. and Adams, Paul D.},
abstractNote = {Stilbenes are diphenyl ethene compounds produced naturally in a wide variety of plant species and some bacteria. Stilbenes are also derived from lignin during kraft pulping. Stilbene cleavage oxygenases (SCOs) cleave the central double bond of stilbenes, forming two phenolic aldehydes. Here in this paper, we report the structure of an SCO. The X-ray structure of NOV1 from Novosphingobium aromaticivorans was determined in complex with its substrate resveratrol (1.89 Å), its product vanillin (1.75 Å), and without any bound ligand (1.61 Å). The enzyme is a seven-bladed β-propeller with an iron cofactor coordinated by four histidines. In all three structures, dioxygen is observed bound to the iron in a side-on fashion. These structures, along with EPR analysis, allow us to propose a mechanism in which a ferric-superoxide reactswith substrate activated by deprotonation of a phenol group at position 4 of the substrate, which allows movement of electron density toward the central double bond and thus facilitates reaction with the ferric superoxide electrophile. Correspondingly, NOV1 cleaves a wide range of other stilbene-like compounds with a 4'-OH group, offering potential in processing some solubilized fragments of lignin into monomer aromatic compounds.},
doi = {10.1073/pnas.1608917113},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 50,
volume = 113,
place = {United States},
year = {2016},
month = {11}
}

Works referenced in this record:

Pathways for degradation of lignin in bacteria and fungi
journal, January 2011
  • Bugg, Timothy D. H.; Ahmad, Mark; Hardiman, Elizabeth M.
  • Natural Product Reports, Vol. 28, Issue 12, p. 1883-1896
  • DOI: 10.1039/c1np00042j

Coot model-building tools for molecular graphics
journal, November 2004
  • Emsley, Paul; Cowtan, Kevin
  • Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132
  • DOI: 10.1107/S0907444904019158

PHENIX: a comprehensive Python-based system for macromolecular structure solution
journal, January 2010
  • Adams, Paul D.; Afonine, Pavel V.; Bunk�czi, G�bor
  • Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221
  • DOI: 10.1107/S0907444909052925