Structure and Mechanism of Ferulic Acid Decarboxylase (FDC1) from Saccharomyces cerevisiae

Bhuiya, Mohammad Wadud; Lee, Soon Goo; Jez, Joseph M.; Yu, Oliver

doi:10.1128/aem.00762-15

Structure and Mechanism of Ferulic Acid Decarboxylase (FDC1) from Saccharomyces cerevisiae

Journal Article · Fri Apr 10 00:00:00 EDT 2015 · Applied and Environmental Microbiology

DOI:https://doi.org/10.1128/aem.00762-15· OSTI ID:1208684

Bhuiya, Mohammad Wadud ^[1]; Lee, Soon Goo ^[2]; Jez, Joseph M. ^[2]; Yu, Oliver ^[3]

Conagen, Inc., Bedford, MA (United States)
Washington Univ., St. Louis, MO (United States)
Conagen, Inc., Bedford, MA (United States); Wuxi NewWay, Jiangsu (China)

The nonoxidative decarboxylation of aromatic acids occurs in a range of microbes and is of interest for bioprocessing and metabolic engineering. Although phenolic acid decarboxylases provide useful tools for bioindustrial applications, the molecular bases for how these enzymes function are only beginning to be examined. Here we present the 2.35-Å-resolution X-ray crystal structure of the ferulic acid decarboxylase (FDC1; UbiD) from Saccharomyces cerevisiae. FDC1 shares structural similarity with the UbiD family of enzymes that are involved in ubiquinone biosynthesis. The position of 4-vinylphenol, the product of p-coumaric acid decarboxylation, in the structure identifies a large hydrophobic cavity as the active site. Differences in the β2e-α5 loop of chains in the crystal structure suggest that the conformational flexibility of this loop allows access to the active site. The structure also implicates Glu285 as the general base in the nonoxidative decarboxylation reaction catalyzed by FDC1. Biochemical analysis showed a loss of enzymatic activity in the E285A mutant. Modeling of 3-methoxy-4-hydroxy-5-decaprenylbenzoate, a partial structure of the physiological UbiD substrate, in the binding site suggests that an ~30-Å-long pocket adjacent to the catalytic site may accommodate the isoprenoid tail of the substrate needed for ubiquinone biosynthesis in yeast. The three-dimensional structure of yeast FDC1 provides a template for guiding protein engineering studies aimed at optimizing the efficiency of aromatic acid decarboxylation reactions in bioindustrial applications.

View Accepted Manuscript (DOE)

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

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

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1208684

Journal Information:: Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 12 Vol. 81; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: ENGLISH

References (47)

A Coenzyme-Independent Decarboxylase/Oxygenase Cascade for the Efficient Synthesis of Vanillin Furuya, Toshiki; Miura, Misa; Kino, Kuniki ChemBioChem, Vol. 15, Issue 15 https://doi.org/10.1002/cbic.201402215	journal	August 2014
AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading Trott, Oleg; Olson, Arthur J. Journal of Computational Chemistry https://doi.org/10.1002/jcc.21334	journal	January 2009
p -Coumaric acid decarboxylase from Lactobacillus plantarum : Structural insights into the active site and decarboxylation catalytic mechanism Rodríguez, Héctor; Angulo, Iván; de las Rivas, Blanca Proteins: Structure, Function, and Bioinformatics https://doi.org/10.1002/prot.22684	journal	January 2010
Stereochemically Specific Proton Transfer in Decarboxylation of 4-Hydroxycinnamic Acids by 4-Hydroxycinnamate Decarboxylase fromKlebsiella oxytoca Hashidoko, Yasuyuki; Tahara, Satoshi Archives of Biochemistry and Biophysics, Vol. 359, Issue 2 https://doi.org/10.1006/abbi.1998.0911	journal	November 1998
New advances in coenzyme Q biosynthesis Clarke, Catherine F. Protoplasma, Vol. 213, Issue 3-4 https://doi.org/10.1007/BF01282151	journal	September 2000
Biochemical studies on cloned Bacillus sp. BP-7 phenolic acid decarboxylase PadA Prim, N.; Pastor, F. I. J.; Diaz, P. Applied Microbiology and Biotechnology, Vol. 63, Issue 1 https://doi.org/10.1007/s00253-003-1371-y	journal	November 2003
Cloning, sequencing, and overexpression in Escherichia coli of the Enterobacter sp. Px6-4 gene for ferulic acid decarboxylase Gu, Wen; Li, Xuemei; Huang, Jingwen Applied Microbiology and Biotechnology, Vol. 89, Issue 6 https://doi.org/10.1007/s00253-010-2978-4	journal	November 2010
Molecular engineering of industrial enzymes: recent advances and future prospects Yang, Haiquan; Li, Jianghua; Shin, Hyun-dong Applied Microbiology and Biotechnology, Vol. 98, Issue 1 https://doi.org/10.1007/s00253-013-5370-3	journal	November 2013
Gene cloning, expression, and characterization of phenolic acid decarboxylase from Lactobacillus brevis RM84 Landete, José María; Rodríguez, Héctor; Curiel, José Antonio Journal of Industrial Microbiology & Biotechnology, Vol. 37, Issue 6 https://doi.org/10.1007/s10295-010-0709-6	journal	March 2010
PAD1 encodes phenylacrylic acid decarboxylase which confers resistance to cinnamic acid in Saccharomyces cerevisiae Clausen, Monika; Lamb, Christopher J.; Megnet, Roland Gene, Vol. 142, Issue 1 https://doi.org/10.1016/0378-1119(94)90363-8	journal	May 1994
Mechanisms of ferulic acid conversions to vanillic acid and guaiacol by Rhodotorula rubra. Huang, Z.; Dostal, L.; Rosazza, J. P. Journal of Biological Chemistry, Vol. 268, Issue 32 https://doi.org/10.1016/S0021-9258(20)80477-3	journal	November 1993
Dehydrogenation of ethylbenzene to styrene over Fe2O3/Al2O3 catalysts in the presence of carbon dioxide Mimura, Naoki; Saito, Masahiro Catalysis Today, Vol. 55, Issue 1-2 https://doi.org/10.1016/S0920-5861(99)00236-9	journal	January 2000
The role of UbiX in Escherichia coli coenzyme Q biosynthesis Gulmezian, Melissa; Hyman, Kyle R.; Marbois, Beth N. Archives of Biochemistry and Biophysics, Vol. 467, Issue 2 https://doi.org/10.1016/j.abb.2007.08.009	journal	November 2007
Pathway and protein engineering approaches to produce novel and commodity small molecules Bhan, Namita; Xu, Peng; Koffas, Mattheos AG Current Opinion in Biotechnology, Vol. 24, Issue 6 https://doi.org/10.1016/j.copbio.2013.02.019	journal	December 2013
PAD1 and FDC1 are essential for the decarboxylation of phenylacrylic acids in Saccharomyces cerevisiae Mukai, Nobuhiko; Masaki, Kazuo; Fujii, Tsutomu Journal of Bioscience and Bioengineering, Vol. 109, Issue 6, p. 564-569 https://doi.org/10.1016/j.jbiosc.2009.11.011	journal	June 2010
Contributions of conserved serine and tyrosine residues to catalysis, ligand binding, and cofactor processing in the active site of tyrosine ammonia lyase Schroeder, Amy C.; Kumaran, Sangaralingam; Hicks, Leslie M. Phytochemistry, Vol. 69, Issue 7, p. 1496-1506 https://doi.org/10.1016/j.phytochem.2008.02.007	journal	May 2008
Distribution of genes encoding the microbial non-oxidative reversible hydroxyarylic acid decarboxylases/phenol carboxylases☆ Lupa, B.; Lyon, D.; Gibbs, M. Genomics, Vol. 86, Issue 3 https://doi.org/10.1016/j.ygeno.2005.05.002	journal	September 2005
Styrene biosynthesis from glucose by engineered E. coli McKenna, Rebekah; Nielsen, David R. Metabolic Engineering, Vol. 13, Issue 5 https://doi.org/10.1016/j.ymben.2011.06.005	journal	September 2011
Enhancing Volatile Phenol Concentrations in Wine by Expressing Various Phenolic Acid Decarboxylase Genes in Saccharomyces cerevisiae Smit, Annél; Cordero Otero, Ricardo R.; Lambrechts, Marius G. Journal of Agricultural and Food Chemistry, Vol. 51, Issue 17 https://doi.org/10.1021/jf026224d	journal	August 2003
Characterization of the p -Coumaric Acid Decarboxylase from Lactobacillus plantarum CECT 748 ^T Rodríguez, Héctor; Landete, José María; Curiel, José Antonio Journal of Agricultural and Food Chemistry, Vol. 56, Issue 9 https://doi.org/10.1021/jf703779s	journal	May 2008
Structural Characterization of Amorfrutins Bound to the Peroxisome Proliferator-Activated Receptor γ de Groot, Jens C.; Weidner, Christopher; Krausze, Joern Journal of Medicinal Chemistry, Vol. 56, Issue 4 https://doi.org/10.1021/jm3013272	journal	February 2013
I-TASSER: a unified platform for automated protein structure and function prediction Roy, Ambrish; Kucukural, Alper; Zhang, Yang Nature Protocols, Vol. 5, Issue 4 https://doi.org/10.1038/nprot.2010.5	journal	March 2010
Dali server: conservation mapping in 3D Holm, Liisa; Rosenstrï¿½m, Pï¿½ivi Nucleic Acids Research, Vol. 38, Issue suppl_2 https://doi.org/10.1093/nar/gkq366	journal	May 2010
Characterization of a vanillic acid non-oxidative decarboxylation gene cluster from Streptomyces sp. D7 The GenBank accession number for the sequence reported in this paper is AF134589. Chow, Kevin T.; Pope, Margaret K.; Davies, Julian Microbiology, Vol. 145, Issue 9 https://doi.org/10.1099/00221287-145-9-2393	journal	September 1999
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
HKL -3000: the integration of data reduction and structure solution – from diffraction images to an initial model in minutes Minor, Wladek; Cymborowski, Marcin; Otwinowski, Zbyszek Acta Crystallographica Section D Biological Crystallography, Vol. 62, Issue 8 https://doi.org/10.1107/S0907444906019949	journal	July 2006
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
Structural analysis of Bacillus pumilus phenolic acid decarboxylase, a lipocalin-fold enzyme Matte, Allan; Grosse, Stephan; Bergeron, Hélène Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 66, Issue 11 https://doi.org/10.1107/S174430911003246X	journal	October 2010
Structure of PA4019, a putative aromatic acid decarboxylase from Pseudomonas aeruginosa Kopec, Jolanta; Schnell, Robert; Schneider, Gunter Acta Crystallographica Section F Structural Biology and Crystallization Communications, Vol. 67, Issue 10 https://doi.org/10.1107/S174430911102923X	journal	September 2011
Crystal structure of a dodecameric FMN-dependent UbiX-like decarboxylase (Pad1) from Escherichia coli O157: H7 Rangarajan, Erumbi S.; Li, Yunge; Iannuzzi, Pietro Protein Science, Vol. 13, Issue 11 https://doi.org/10.1110/ps.04953004	journal	November 2004
Nature’s assembly line: biosynthesis of simple phenylpropanoids and polyketides Yu, Oliver; Jez, Joseph M. The Plant Journal, Vol. 54, Issue 4 https://doi.org/10.1111/j.1365-313X.2008.03436.x	journal	May 2008
Metabolism of Ferulic Acid by Paecilomyces variotii and Pestalotia palmarum Rahouti, Mohammed; Seigle-Murandi, Françoise; Steiman, Régine Applied and Environmental Microbiology, Vol. 55, Issue 9 https://doi.org/10.1128/AEM.55.9.2391-2398.1989	journal	January 1989
Purification and characterization of ferulate and p-coumarate decarboxylase from Bacillus pumilus. Degrassi, G.; Polverino De Laureto, P.; Bruschi, C. V. Applied and environmental microbiology, Vol. 61, Issue 1 https://doi.org/10.1128/AEM.61.1.326-332.1995	journal	January 1995
Cloning, sequencing, and expression in Escherichia coli of the Bacillus pumilus gene for ferulic acid decarboxylase. Zago, A.; Degrassi, G.; Bruschi, C. V. Applied and environmental microbiology, Vol. 61, Issue 12 https://doi.org/10.1128/AEM.61.12.4484-4486.1995	journal	January 1995
Gene Cloning, Transcriptional Analysis, Purification, and Characterization of Phenolic Acid Decarboxylase from Bacillus subtilis Cavin, Jean-François; Dartois, Véronique; Diviès, Charles Applied and Environmental Microbiology, Vol. 64, Issue 4 https://doi.org/10.1128/AEM.64.4.1466-1471.1998	journal	April 1998
Expression in Escherichia coli of Native and Chimeric Phenolic Acid Decarboxylases with Modified Enzymatic Activities and Method for Screening Recombinant E. coli Strains Expressing These Enzymes Barthelmebs, Lise; Diviès, Charles; Cavin, Jean-François Applied and Environmental Microbiology, Vol. 67, Issue 3 https://doi.org/10.1128/AEM.67.3.1063-1069.2001	journal	March 2001
Identification of the ubiD Gene on theEscherichia coli Chromosome Zhang, Haitao; Javor, George T. Journal of Bacteriology, Vol. 182, Issue 21 https://doi.org/10.1128/JB.182.21.6243-6246.2000	journal	November 2000
Metabolism of Ferulic Acid by Paecilomyces variotii and Pestalotia palmarum Rahouti, Mohammed; Seigle-Murandi, Françoise; Steiman, Régine Applied and Environmental Microbiology, Vol. 55, Issue 9 https://doi.org/10.1128/aem.55.9.2391-2398.1989	journal	January 1989
Purification and characterization of ferulate and p-coumarate decarboxylase from Bacillus pumilus. Degrassi, G.; Polverino De Laureto, P.; Bruschi, C. V. Applied and environmental microbiology, Vol. 61, Issue 1 https://doi.org/10.1128/aem.61.1.326-332.1995	journal	January 1995
Cloning, sequencing, and expression in Escherichia coli of the Bacillus pumilus gene for ferulic acid decarboxylase. Zago, A.; Degrassi, G.; Bruschi, C. V. Applied and environmental microbiology, Vol. 61, Issue 12 https://doi.org/10.1128/aem.61.12.4484-4486.1995	journal	January 1995
Purification and characterization of a ferulic acid decarboxylase from Pseudomonas fluorescens. Huang, Z.; Dostal, L.; Rosazza, J. P. Journal of Bacteriology, Vol. 176, Issue 19 https://doi.org/10.1128/jb.176.19.5912-5918.1994	journal	January 1994
Biocatalytic Syntheses of Aromatics from D-Glucose: Renewable Microbial Sources of Aromatic Compounds Frost, J. W.; Draths, K. M. Annual Review of Microbiology, Vol. 49, Issue 1 https://doi.org/10.1146/annurev.mi.49.100195.003013	journal	October 1995
Rapid isolation of yeast genomic DNA: Bust n' Grab Harju, Susanna; Fedosyuk, Halyna; Peterson, Kenneth R. BMC Biotechnology, Vol. 4, Issue 1, p. 8 https://doi.org/10.1186/1472-6750-4-8	journal	January 2004
Rational and combinatorial approaches to engineering styrene production by Saccharomyces cerevisiae McKenna, Rebekah; Thompson, Brian; Pugh, Shawn Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/s12934-014-0123-2	journal	August 2014
Structural Basis of Enzymatic Activity for the Ferulic Acid Decarboxylase (FADase) from Enterobacter sp. Px6-4 Gu, Wen; Yang, Jinkui; Lou, Zhiyong PLoS ONE, Vol. 6, Issue 1 https://doi.org/10.1371/journal.pone.0016262	journal	January 2011
Structural Insights into the UbiD Protein Family from the Crystal Structure of PA0254 from Pseudomonas aeruginosa Jacewicz, Agata; Izumi, Atsushi; Brunner, Katharina PLoS ONE, Vol. 8, Issue 5 https://doi.org/10.1371/journal.pone.0063161	journal	May 2013

Cited By (10)

Effect of Bacterial and Yeast Starters on the Formation of Volatile and Organic Acid Compounds in Coffee Beans and Selection of Flavors Markers Precursors During Wet Fermentation Martinez, Silvia Juliana; Bressani, Ana Paula Pereira; Dias, Disney Ribeiro Frontiers in Microbiology, Vol. 10 https://doi.org/10.3389/fmicb.2019.01287	journal	June 2019
Changes in the content of free phenolic acids and antioxidative capacity of wholemeal bread in relation to cereal species and fermentation type Skrajda-Brdak, Marta; Konopka, Iwona; Tańska, Małgorzata European Food Research and Technology, Vol. 245, Issue 10 https://doi.org/10.1007/s00217-019-03331-y	journal	July 2019
Exploring the substrate scope of ferulic acid decarboxylase (FDC1) from Saccharomyces cerevisiae Nagy, Emma Zsófia Aletta; Nagy, Csaba Levente; Filip, Alina Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-36977-x	journal	January 2019
Biologically generated carbon dioxide: nature's versatile chemical strategies for carboxy lyases Walsh, Christopher T. Natural Product Reports, Vol. 37, Issue 1 https://doi.org/10.1039/c9np00015a	journal	January 2020
Enzymes involved in the anaerobic degradation of ortho -phthalate by the nitrate-reducing bacterium Azoarcus sp. strain PA01 : Anaerobic Junghare, Madan; Spiteller, Dieter; Schink, Bernhard Environmental Microbiology, Vol. 18, Issue 9 https://doi.org/10.1111/1462-2920.13447	journal	August 2016
Phthaloyl-coenzyme A decarboxylase from Thauera chlorobenzoica : the prenylated flavin-, K ⁺ - and Fe ²⁺ -dependent key enzyme of anaerobic phthalate degradation: UbiD-like phthaloyl-CoA decarboxylase Mergelsberg, Mario; Willistein, Max; Meyer, Heike Environmental Microbiology, Vol. 19, Issue 9 https://doi.org/10.1111/1462-2920.13875	journal	August 2017
Chemical genomic guided engineering of gamma-valerolactone tolerant yeast Bottoms, Scott; Dickinson, Quinn; McGee, Mick Microbial Cell Factories, Vol. 17, Issue 1 https://doi.org/10.1186/s12934-017-0848-9	journal	January 2018
Reducing phenolic off-flavors through CRISPR-based gene editing of the FDC1 gene in Saccharomyces cerevisiae x Saccharomyces eubayanus hybrid lager beer yeasts Mertens, Stijn; Gallone, Brigida; Steensels, Jan PLOS ONE, Vol. 14, Issue 1 https://doi.org/10.1371/journal.pone.0209124	journal	January 2019
Selection of Pof-Saccharomyces eubayanus Variants for the Construction of S. cerevisiae × S. eubayanus Hybrids With Reduced 4-Vinyl Guaiacol Formation Diderich, Jasper A.; Weening, Susan M.; van den Broek, Marcel Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01640	journal	July 2018
The Impact of Simple Phenolic Compounds on Beer Aroma and Flavor Lentz, Michael Fermentation, Vol. 4, Issue 1 https://doi.org/10.3390/fermentation4010020	journal	March 2018

Similar Records

Biochemical and Structural Characterization of TtnD, a Prenylated FMN-Dependent Decarboxylase from the Tautomycetin Biosynthetic Pathway

Journal Article · Tue Aug 28 00:00:00 EDT 2018 · ACS Chemical Biology · OSTI ID:1476086

Related Subjects

59 BASIC BIOLOGICAL SCIENCES

Structure and Mechanism of Ferulic Acid Decarboxylase (FDC1) from Saccharomyces cerevisiae

Citation Formats

References (47)

Cited By (10)

Similar Records

Related Subjects