Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway

Gall, Daniel L.; Kim, Hoon; Lu, Fachuang; Donohue, Timothy J.; Noguera, Daniel R.; Ralph, John

doi:10.1074/jbc.m113.536250

Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway

Journal Article · Thu Feb 06 23:00:00 EST 2014 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.m113.536250· OSTI ID:1904221

Gall, Daniel L. ^[1]; Kim, Hoon ^[2]; Lu, Fachuang ^[2]; Donohue, Timothy J. ^[2]; Noguera, Daniel R. ^[2]; Ralph, John ^[2]

University of Wisconsin, Madison, WI (United States); Univ. of Wisconsin, Madison, WI (United States)
University of Wisconsin, Madison, WI (United States)

Glutathione-dependent enzymes play important protective, repair, or metabolic roles in cells. In particular, enzymes in the glutathione S-transferase (GST) superfamily function in stress responses, defense systems, or xenobiotic detoxification. Here, we identify novel features of bacterial GSTs that cleave -aryl ether bonds typically found in plant lignin. Our data reveal several original features of the reaction cycle of these GSTs, including stereospecific substrate recognition and stereoselective formation of -S-thioether linkages. Products of recombinant GSTs (LigE, LigP, and LigF) are -S-glutathionyl--ketothioethers that are degraded by a -S-thioetherase (LigG). All three Lig GSTs produced the ketone product (-S-glutathionyl- -veratrylethanone) from an achiral side chain-truncated model substrate (-guaiacyl--veratrylethanone). However, when -etherase assays were conducted with a racemic model substrate, -guaiacyl--veratrylglycerone, LigE- or LigP-catalyzed reactions yielded only one of two potential product (-Sglutathionyl--veratrylglycerone) epimers, whereas the other diastereomer (differing in configuration at the -position (i.e. its-epimer)) was produced only in the LigF-catalyzed reaction. Thus, -etherase catalysis causes stereochemical inversion of the chiral center, converting a (R)-substrate to a (S)-product (LigE and LigP), and a (S)-substrate to a (R)-product (LigF). Further, LigG catalyzed glutathione-dependent -S-thioether cleavage with-S-glutathionyl--veratrylethanone and with(R)- configured -S-glutathionyl--veratrylglycerone but exhibited no or significantly reduced -S-thioether-cleaving activity with the (S)-epimer, demonstrating that LigG is a stereospecific -thioetherase. We therefore propose that multiple Lig enzymes are needed in this -aryl etherase pathway in order to cleave the racemic -ether linkages that are present in the backbone of the lignin polymer.

View Accepted Manuscript (DOE)

Research Organization:: University of Wisconsin, Madison, WI (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: FC02-07ER64494

OSTI ID:: 1904221

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Journal Issue: 12 Vol. 289; ISSN 0021-9258

Publisher:: American Society for Biochemistry and Molecular BiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (51)

Biochemical and mutational analysis of a plant virus polyprotein cleavage site. Dougherty, W. G.; Carrington, J. C.; Cary, S. M. The EMBO Journal, Vol. 7, Issue 5 https://doi.org/10.1002/j.1460-2075.1988.tb02942.x	journal	May 1988
Detection and localization of a new enzyme catalyzing the β-aryl ether cleavage in the soil bacterium ( Pseudomonas paucimobilis SYK-6) Masai, Eiji; Katayama, Yoshihiro; Nishikawa, Seiji FEBS Letters, Vol. 249, Issue 2 https://doi.org/10.1016/0014-5793(89)80656-8	journal	June 1989
Molecular genetic analysis of a plant virus polyprotein cleavage site: A model Dougherty, William G.; Cary, Susan M.; Dawn Parks, T. Virology, Vol. 171, Issue 2 https://doi.org/10.1016/0042-6822(89)90603-x	journal	August 1989
Post-translational processing of the tobacco etch virus 49-kDa small nuclear inclusion polyprotein: Identification of an internal cleavage site and delimitation of VPg and proteinase domains Dougherty, William G.; Dawn Parks, T. Virology, Vol. 183, Issue 2 https://doi.org/10.1016/0042-6822(91)90974-g	journal	August 1991
A combined approach to improving large-scale production of tobacco etch virus protease Blommel, Paul G.; Fox, Brian G. Protein Expression and Purification, Vol. 55, Issue 1, p. 53-68 https://doi.org/10.1016/j.pep.2007.04.013	journal	September 2007
Glutathione transferases: new functions Oakley, Aaron J. Current Opinion in Structural Biology, Vol. 15, Issue 6 https://doi.org/10.1016/j.sbi.2005.10.005	journal	December 2005
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
Are Lignins Optically Active? Ralph, John; Peng, Junpeng; Lu, Fachuang Journal of Agricultural and Food Chemistry, Vol. 47, Issue 8 https://doi.org/10.1021/jf9901136	journal	August 1999
Mechanistic and structural insights into the proteolytic activation of Vibrio cholerae MARTX toxin Shen, Aimee; Lupardus, Patrick J.; Albrow, Victoria E. Nature Chemical Biology, Vol. 5, Issue 7 https://doi.org/10.1038/nchembio.178	journal	May 2009
Construction of long DNA molecules using long PCR-based fusion of several fragments simultaneously Shevchuk, N. A. Nucleic Acids Research, Vol. 32, Issue 2 https://doi.org/10.1093/nar/gnh014	journal	January 2004
Stress-Induced Phenylpropanoid Metabolism. Dixon, R. A.; Paiva, N. L. The Plant Cell https://doi.org/10.1105/tpc.7.7.1085	journal	July 1995
Identification of Three Alcohol Dehydrogenase Genes Involved in the Stereospecific Catabolism of Arylglycerol- -Aryl Ether by Sphingobium sp. Strain SYK-6 Sato, Y.; Moriuchi, H.; Hishiyama, S. Applied and Environmental Microbiology, Vol. 75, Issue 16 https://doi.org/10.1128/aem.00880-09	journal	June 2009
Bacterial glutathione S-transferases: what are they good for? Vuilleumier, S. Journal of Bacteriology, Vol. 179, Issue 5 https://doi.org/10.1128/jb.179.5.1431-1441.1997	journal	March 1997
The 4-Oxalomesaconate Hydratase Gene, Involved in the Protocatechuate 4,5-Cleavage Pathway, Is Essential to Vanillate and Syringate Degradation in Sphingomonas paucimobilis SYK-6 Hara, Hirofumi; Masai, Eiji; Katayama, Yoshihiro Journal of Bacteriology, Vol. 182, Issue 24 https://doi.org/10.1128/jb.182.24.6950-6957.2000	journal	December 2000
Roles of the Enantioselective Glutathione S-Transferases in Cleavage of -Aryl Ether Masai, E.; Ichimura, A.; Sato, Y. Journal of Bacteriology, Vol. 185, Issue 6 https://doi.org/10.1128/jb.185.6.1768-1775.2003	journal	March 2003
Lysogeny at Mid-Twentieth Century: P1, P2, and Other Experimental Systems Bertani, G. Journal of Bacteriology, Vol. 186, Issue 3 https://doi.org/10.1128/jb.186.3.595-600.2004	journal	January 2004
Studies on Lysogenesis i. Bertani, G. Journal of Bacteriology, Vol. 62, Issue 3 https://doi.org/10.1128/jb.62.3.293-300.1951	journal	January 1951
Mutational analysis of tobacco etch virus polyprotein processing: cis and trans proteolytic activities of polyproteins containing the 49-kilodalton proteinase Carrington, J. C.; Cary, S. M.; Dougherty, W. G. Journal of Virology, Vol. 62, Issue 7 https://doi.org/10.1128/jvi.62.7.2313-2320.1988	journal	July 1988
Lignin: Occurrence, Biogenesis and Biodegradation Lewis, N. G.; Yamamoto, E. Annual Review of Plant Physiology and Plant Molecular Biology, Vol. 41, Issue 1 https://doi.org/10.1146/annurev.pp.41.060190.002323	journal	June 1990
Characterization of the Third Glutathione S -Transferase Gene Involved in Enantioselective Cleavage of the β-Aryl Ether by Sphingobium sp. Strain SYK-6 Tanamura, Kazuyuki; Abe, Tomokuni; Kamimura, Naofumi Bioscience, Biotechnology, and Biochemistry, Vol. 75, Issue 12 https://doi.org/10.1271/bbb.110525	journal	December 2011
Characterization of the Cα-Dehydrogenase Gene Involved in the Cleavage of β-Aryl Ether by Pseudomonas paucimobilis Masai, Eiji; Kubota, Sachiko; Katayama, Yoshihiro Bioscience, Biotechnology, and Biochemistry, Vol. 57, Issue 10 https://doi.org/10.1271/bbb.57.1655	journal	January 1993
Genetic and Biochemical Investigations on Bacterial Catabolic Pathways for Lignin-Derived Aromatic Compounds Masai, Eiji; Katayama, Yoshihiro; Fukuda, Masao Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 1 https://doi.org/10.1271/bbb.60437	journal	January 2007
Simplified, Enhanced Protein Purification Using an Inducible, Autoprocessing Enzyme Tag Shen, Aimee; Lupardus, Patrick J.; Morell, Montse PLoS ONE, Vol. 4, Issue 12 https://doi.org/10.1371/journal.pone.0008119	journal	December 2009
Methods in 2012, part 2 Blow, Nathan S. BioTechniques, Vol. 53, Issue 1 https://doi.org/10.2144/000113882	journal	July 2012
Lignin chemistry?past, present and future Adler, Erich Wood Science and Technology, Vol. 11, Issue 3 https://doi.org/10.1007/BF00365615	journal	January 1977
Erythro/threo ratio ofβ-O-4 structures as an important structural characteristic of lignin. I: Improvement of ozonation method for the quantitative analysis of lignin side-chain structure Akiyama, Takuya; Sugimoto, Tomoko; Matsumoto, Yuji Journal of Wood Science, Vol. 48, Issue 3 https://doi.org/10.1007/BF00771369	journal	June 2002
Proof of the presence of racemic forms of arylglycerol-Β-aryl ether structure in lignin: studies on the stereo structure of lignin by ozonation Akiyama, Takuya; Magara, Kengo; Matsumoto, Yuji Journal of Wood Science, Vol. 46, Issue 5 https://doi.org/10.1007/BF00776407	journal	October 2000
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Bradford, Marion M. Analytical Biochemistry, Vol. 72, Issue 1-2 https://doi.org/10.1016/0003-2697(76)90527-3	journal	May 1976
A bacterial enzyme degrading the model lignin compound β-etherase is a member of the glutathione- S -transferase superfamily Masai, Eiji; Katayama, Yoshihiro; Kubota, Sachiko FEBS Letters, Vol. 323, Issue 1-2 https://doi.org/10.1016/0014-5793(93)81465-C	journal	May 1993
Molecular genetic analysis of a plant virus polyprotein cleavage site: A model Dougherty, William G.; Cary, Susan M.; Dawn Parks, T. Virology, Vol. 171, Issue 2 https://doi.org/10.1016/0042-6822(89)90603-X	journal	August 1989
Post-translational processing of the tobacco etch virus 49-kDa small nuclear inclusion polyprotein: Identification of an internal cleavage site and delimitation of VPg and proteinase domains Dougherty, William G.; Dawn Parks, T. Virology, Vol. 183, Issue 2 https://doi.org/10.1016/0042-6822(91)90974-G	journal	August 1991
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
Advances in modifying lignin for enhanced biofuel production Simmons, Blake A.; Loqué, Dominique; Ralph, John Current Opinion in Plant Biology, Vol. 13, Issue 3, p. 312-319 https://doi.org/10.1016/j.pbi.2010.03.001	journal	June 2010
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Convenient synthesis of chiral lignin model compounds via optical resolution: four stereoisomers of guaiacylglycerol-β-guaiacyl ether and both enantiomers of 3-hydroxy-1-(4-hydroxy-3-methoxyphenyl)-2-(2-methoxyphenoxy)-propan-1-one (erone) Hishiyama, Shojiro; Otsuka, Yuichiro; Nakamura, Masaya Tetrahedron Letters, Vol. 53, Issue 7 https://doi.org/10.1016/j.tetlet.2011.12.016	journal	February 2012
Derivatization Followed by Reductive Cleavage (DFRC Method), a New Method for Lignin Analysis: Protocol for Analysis of DFRC Monomers Lu, Fachuang; Ralph, John Journal of Agricultural and Food Chemistry, Vol. 45, Issue 7 https://doi.org/10.1021/jf970258h	journal	July 1997
DFRC Method for Lignin Analysis. 1. New Method for β-Aryl Ether Cleavage: Lignin Model Studies Lu, Fachuang; Ralph, John Journal of Agricultural and Food Chemistry, Vol. 45, Issue 12 https://doi.org/10.1021/jf970539p	journal	December 1997
Biosynthesis and Constitution of Lignin Freudenberg, Karl Nature, Vol. 183, Issue 4669 https://doi.org/10.1038/1831152a0	journal	April 1959
Autoprocessing of the Vibrio cholerae RTX toxin by the cysteine protease domain Sheahan, Kerri-Lynn; Cordero, Christina L.; Satchell, Karla J. Fullner The EMBO Journal, Vol. 26, Issue 10 https://doi.org/10.1038/sj.emboj.7601700	journal	April 2007
Structure, function and evolution of glutathione transferases: implications for classification of non-mammalian members of an ancient enzyme superfamily Sheehan, David; Meade, Gerardene; Foley, Vivienne M. Biochemical Journal, Vol. 360, Issue 1 https://doi.org/10.1042/bj3600001	journal	November 2001
Structural and Molecular Mechanism for Autoprocessing of MARTX Toxin of Vibrio cholerae at Multiple Sites Prochazkova, Katerina; Shuvalova, Ludmilla A.; Minasov, George Journal of Biological Chemistry, Vol. 284, Issue 39 https://doi.org/10.1074/jbc.M109.025510	journal	September 2009
Identification of Three Alcohol Dehydrogenase Genes Involved in the Stereospecific Catabolism of Arylglycerol- -Aryl Ether by Sphingobium sp. Strain SYK-6 Sato, Y.; Moriuchi, H.; Hishiyama, S. Applied and Environmental Microbiology, Vol. 75, Issue 16 https://doi.org/10.1128/AEM.00880-09	journal	June 2009
The 4-Oxalomesaconate Hydratase Gene, Involved in the Protocatechuate 4,5-Cleavage Pathway, Is Essential to Vanillate and Syringate Degradation in Sphingomonas paucimobilis SYK-6 Hara, Hirofumi; Masai, Eiji; Katayama, Yoshihiro Journal of Bacteriology, Vol. 182, Issue 24 https://doi.org/10.1128/JB.182.24.6950-6957.2000	journal	December 2000
Roles of the Enantioselective Glutathione S-Transferases in Cleavage of -Aryl Ether Masai, E.; Ichimura, A.; Sato, Y. Journal of Bacteriology, Vol. 185, Issue 6 https://doi.org/10.1128/JB.185.6.1768-1775.2003	journal	March 2003
Lysogeny at Mid-Twentieth Century: P1, P2, and Other Experimental Systems Bertani, G. Journal of Bacteriology, Vol. 186, Issue 3 https://doi.org/10.1128/JB.186.3.595-600.2004	journal	January 2004
Cloning and sequencing of the gene for a Pseudomonas paucimobilis enzyme that cleaves beta-aryl ether. Masai, E.; Katayama, Y.; Kawai, S. Journal of Bacteriology, Vol. 173, Issue 24 https://doi.org/10.1128/jb.173.24.7950-7955.1991	journal	January 1991
Glutathione Transferases Hayes, John D.; Flanagan, Jack U.; Jowsey, Ian R. Annual Review of Pharmacology and Toxicology, Vol. 45, Issue 1 https://doi.org/10.1146/annurev.pharmtox.45.120403.095857	journal	September 2005
Overlap extension PCR cloning: a simple and reliable way to create recombinant plasmids Bryksin, Anton; Matsumura, Ichiro BioTechniques, Vol. 48, Issue 6 https://doi.org/10.2144/000113418	journal	June 2010
Gene Splicing by Overlap Extension: Tailor-Made Genes Using the Polymerase Chain Reaction Horton, Robert M.; Cai, Zeling; Ho, Steffan N. BioTechniques, Vol. 54, Issue 3 https://doi.org/10.2144/000114017	journal	March 2013
Stress-Induced Phenylpropanoid Metabolism Dixon, Richard A.; Paiva, Nancy L. The Plant Cell, Vol. 7, Issue 7 https://doi.org/10.2307/3870059	journal	July 1995
Guaiacylglycerol and its beta-Guaiacyl Ether. Adler, Erich; Eriksoo, Edgar; Boss, Ernst Acta Chemica Scandinavica, Vol. 9 https://doi.org/10.3891/acta.chem.scand.09-0341	journal	January 1955

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Stereochemical Features of Glutathione-dependent Enzymes in the Sphingobium sp. Strain SYK-6 β-Aryl Etherase Pathway

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