Stereoinversion via Alcohol Dehydrogenases Enables Complete Catabolism of β-1-Type Lignin-Derived Aromatic Isomers

Kato, Ryo; Maekawa, Kodai; Kobayashi, Shota; Hishiyama, Shojiro; Katahira, Rui; Nambo, Miki; Higuchi, Yudai; Kuatsjah, Eugene; Beckham, Gregg T.; Kamimura, Naofumi; Masai, Eiji

doi:10.1128/aem.00171-23

Title: Stereoinversion via Alcohol Dehydrogenases Enables Complete Catabolism of β-1-Type Lignin-Derived Aromatic Isomers

Journal Article · 14 May 2023 · Applied and Environmental Microbiology

DOI: https://doi.org/10.1128/aem.00171-23 · OSTI ID:1984226

^[1]; Maekawa, Kodai ^[1]; Kobayashi, Shota ^[1]; Hishiyama, Shojiro ^[2];

^[3]; Nambo, Miki ^[1];

^[1];

^[3];

^[1];

^[1]

Nagaoka University of Technology (Japan)
Forestry and Forest Products Research Institute (Japan)
National Renewable Energy Laboratory (NREL), Golden, CO (United States). Renewable Resources and Enabling Science Center

Sphingobium sp. strain SYK-6 is an efficient aromatic catabolic bacterium that can consume all four stereoisomers of 1,2-diguaiacylpropane-1,3-diol (DGPD), which is a ring-opened β-1-type dimer. Recently, LdpA-mediated catabolism of erythro-DGPD was reported in SYK-6, but the catabolic pathway for threo-DGPD was as yet unknown. Here, in this study, we elucidated the catabolism of threo-DGPD, which proceeds through conversion to erythro-DGPD. When threo-DGPD was incubated with SYK-6, the Cα hydroxy groups of threo-DGPD (DGPD I and II) were initially oxidized to produce the Cα carbonyl form (DGPD-keto I and II). This initial oxidation step is catalyzed by Cα-dehydrogenases, which belong to the short-chain dehydrogenase/reductase (SDR) family and are involved in the catabolism of β-O-4-type dimers. Analysis of seven candidate genes revealed that NAD⁺-dependent LigD and LigL are mainly involved in the conversion of DGPD I and II, respectively. Next, we found that DGPD-keto I and II were reduced to erythro-DGPD (DGPD III and IV) in the presence of NADPH. Genes involved in this reduction were sought from Cα-dehydrogenase and ldpA-neighboring SDR genes. The gene products of SLG_12690 (ldpC) and SLG_12640 (ldpB) catalyzed the NADPH-dependent conversion of DGPD-keto I to DGPD III and DGPD-keto II to DGPD IV, respectively. Mutational analysis further indicated that ldpC and ldpB are predominantly involved in the reduction of DGPD-keto. Together, these results demonstrate that SYK-6 harbors a comprehensive catabolic enzyme system to utilize all four β-1-type stereoisomers through successive oxidation and reduction reactions of the Cα hydroxy group of threo-DGPD with a net stereoinversion using multiple dehydrogenases.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Office of Sustainable Transportation. Bioenergy Technologies Office (BETO); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC36-08GO28308

OSTI ID:: 1984226

Report Number(s):: NREL/JA-2A00-86481; MainId:87254; UUID:74935807-3d60-4ae4-b133-fbb1bc3446f6; MainAdminID:69711

Journal Information:: Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 6 Vol. 89; ISSN 0099-2240

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

References (49)

The Substrate Spectrum of Mandelate Racemase: Minimum Structural Requirements for Substrates and Substrate Model Felfer, Ulfried; Goriup, Marian; Koegl, Marion F. Advanced Synthesis & Catalysis, Vol. 347, Issue 7-8 https://doi.org/10.1002/adsc.200505012	journal	June 2005
Lignin Depolymerization and Conversion A Review of Thermochemical Methods Pandey, M. P.; Kim, C. S. Chemical Engineering & Technology, Vol. 34, Issue 1, p. 29-41 https://doi.org/10.1002/ceat.201000270	journal	November 2010
Improved Broad-Host-Range RK2 Vectors Useful for High and Low Regulated Gene Expression Levels in Gram-Negative Bacteria Blatny, Janet Martha; Brautaset, Trygve; Winther-Larsen, Hanne C. Plasmid, Vol. 38, Issue 1 https://doi.org/10.1006/plas.1997.1294	journal	July 1997
Efficient production of 2-pyrone 4,6-dicarboxylic acid as a novel polymer-based material from protocatechuate by microbial function Otsuka, Yuichiro; Nakamura, Masaya; Shigehara, Kiyotaka Applied Microbiology and Biotechnology, Vol. 71, Issue 5 https://doi.org/10.1007/s00253-005-0203-7	journal	December 2005
Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes Studier, F. William; Moffatt, Barbara A. Journal of Molecular Biology, Vol. 189, Issue 1, p. 113-130 https://doi.org/10.1016/0022-2836(86)90385-2	journal	May 1986
Mild hydrogenolysis of in-situ and isolated Pinus radiata lignins Torr, Kirk M.; van de Pas, Daniel J.; Cazeils, Emmanuel Bioresource Technology, Vol. 102, Issue 16 https://doi.org/10.1016/j.biortech.2011.05.040	journal	August 2011
Biological valorization of low molecular weight lignin Abdelaziz, Omar Y.; Brink, Daniel P.; Prothmann, Jens Biotechnology Advances, Vol. 34, Issue 8 https://doi.org/10.1016/j.biotechadv.2016.10.001	journal	December 2016
A field of dreams: Lignin valorization into chemicals, materials, fuels, and health-care products Becker, Judith; Wittmann, Christoph Biotechnology Advances, Vol. 37, Issue 6 https://doi.org/10.1016/j.biotechadv.2019.02.016	journal	November 2019
Enzymatic conversion of lignin into renewable chemicals Bugg, Timothy DH; Rahmanpour, Rahman Current Opinion in Chemical Biology, Vol. 29 https://doi.org/10.1016/j.cbpa.2015.06.009	journal	December 2015
Opportunities and challenges in biological lignin valorization Beckham, Gregg T.; Johnson, Christopher W.; Karp, Eric M. Current Opinion in Biotechnology, Vol. 42 https://doi.org/10.1016/j.copbio.2016.02.030	journal	December 2016
Reductive catalytic fractionation: state of the art of the lignin-first biorefinery Renders, Tom; Van den Bossche, Gil; Vangeel, Thijs Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2018.12.005	journal	April 2019
Lignin structure and its engineering Ralph, John; Lapierre, Catherine; Boerjan, Wout Current Opinion in Biotechnology, Vol. 56 https://doi.org/10.1016/j.copbio.2019.02.019	journal	April 2019
Discovery of pinoresinol reductase genes in sphingomonads Fukuhara, Y.; Kamimura, N.; Nakajima, M. Enzyme and Microbial Technology, Vol. 52, Issue 1 https://doi.org/10.1016/j.enzmictec.2012.10.004	journal	January 2013
Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class Meux, Edgar; Prosper, Pascalita; Masai, Eiji FEBS Letters, Vol. 586, Issue 22 https://doi.org/10.1016/j.febslet.2012.09.036	journal	October 2012
Innovative Chemicals and Materials from Bacterial Aromatic Catabolic Pathways Johnson, Christopher W.; Salvachúa, Davinia; Rorrer, Nicholas A. Joule, Vol. 3, Issue 6 https://doi.org/10.1016/j.joule.2019.05.011	journal	June 2019
Pathway discovery and engineering for cleavage of a β-1 lignin-derived biaryl compound Presley, Gerald N.; Werner, Allison Z.; Katahira, Rui Metabolic Engineering, Vol. 65 https://doi.org/10.1016/j.ymben.2021.02.003	journal	May 2021
Guiding stars to the field of dreams: Metabolically engineered pathways and microbial platforms for a sustainable lignin-based industry Weiland, Fabia; Kohlstedt, Michael; Wittmann, Christoph Metabolic Engineering, Vol. 71 https://doi.org/10.1016/j.ymben.2021.11.011	journal	May 2022
Characterization of the Interunit Bonds of Lignin Oligomers Released by Acid-Catalyzed Selective Solvolysis of Cryptomeria japonica and Eucalyptus globulus Woods via Thioacidolysis and 2D-NMR Saito, Kaori; Kaiho, Atsushi; Sakai, Ryo Journal of Agricultural and Food Chemistry, Vol. 64, Issue 48 https://doi.org/10.1021/acs.jafc.6b04263	journal	November 2016
Catalytic Mechanism of Aryl-Ether Bond Cleavage in Lignin by LigF and LigG Prates, Erica Teixeira; Crowley, Michael F.; Skaf, Munir S. The Journal of Physical Chemistry B, Vol. 123, Issue 48 https://doi.org/10.1021/acs.jpcb.9b06243	journal	November 2019
Mandelate pathway of Pseudomonas putida: sequence relationships involving mandelate racemase, (S)-mandelate dehydrogenase, and benzoylformate decarboxylase and expression of benzoylformate decarboxylase in Escherichia coli Tsou, Amy Y.; Ransom, Stephen C.; Gerlt, John A. Biochemistry, Vol. 29, Issue 42 https://doi.org/10.1021/bi00494a015	journal	October 1990
Orchestration of Concurrent Oxidation and Reduction Cycles for Stereoinversion and Deracemisation of sec -Alcohols Voss, Constance V.; Gruber, Christian C.; Faber, Kurt Journal of the American Chemical Society, Vol. 130, Issue 42 https://doi.org/10.1021/ja804816a	journal	September 2008
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
Roles of two glutathione S-transferases in the final step of the β-aryl ether cleavage pathway in Sphingobium sp. strain SYK-6 Higuchi, Yudai; Sato, Daisuke; Kamimura, Naofumi Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-77462-8	journal	November 2020
Critical enzyme reactions in aromatic catabolism for microbial lignin conversion Erickson, Erika; Bleem, Alissa; Kuatsjah, Eugene Nature Catalysis, Vol. 5, Issue 2 https://doi.org/10.1038/s41929-022-00747-w	journal	February 2022
Chapter 11. Biological Funneling as a Means of Transforming Lignin-derived Aromatic Compounds into Value-added Chemicals Eltis, Lindsay D.; Singh, Rahul Energy and Environment Series https://doi.org/10.1039/9781788010351-00290	book	January 2018
Reductive lignocellulose fractionation into soluble lignin-derived phenolic monomers and dimers and processable carbohydrate pulps Van den Bosch, S.; Schutyser, W.; Vanholme, R. Energy & Environmental Science, Vol. 8, Issue 6 https://doi.org/10.1039/C5EE00204D	journal	January 2015
Biochemical and structural characterization of a sphingomonad diarylpropane lyase for cofactorless deformylation Kuatsjah, Eugene; Zahn, Michael; Chen, Xiangyang Proceedings of the National Academy of Sciences, Vol. 120, Issue 4 https://doi.org/10.1073/pnas.2212246120	journal	January 2023
Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans Figurski, D. H.; Helinski, D. R. Proceedings of the National Academy of Sciences, Vol. 76, Issue 4 https://doi.org/10.1073/pnas.76.4.1648	journal	April 1979
NMR Studies on the Occurrence of Spirodienone Structures in Lignins Zhang, Liming; Gellerstedt, Göran; Ralph, John Journal of Wood Chemistry and Technology, Vol. 26, Issue 1 https://doi.org/10.1080/02773810600580271	journal	April 2006
17β‐Hydroxysteroid dehydrogenase type 8 and carbonyl reductase type 4 assemble as a ketoacyl reductase of human mitochondrial FAS Chen, Zhijun; Kastaniotis, Alexander J.; Miinalainen, Ilkka J. The FASEB Journal, Vol. 23, Issue 11 https://doi.org/10.1096/fj.09-133587	journal	July 2009
Isolation, Characterization and Mapping of Mandelate Pathway Mutants of Acinetobacter calcoaceticus Vakeria, D.; Vivian, A.; Fewson, C. A. Microbiology, Vol. 130, Issue 11 https://doi.org/10.1099/00221287-130-11-2893	journal	November 1984
Lignin Biosynthesis and Structure Vanholme, R.; Demedts, B.; Morreel, K. Plant Physiology, Vol. 153, Issue 3, p. 895-905 https://doi.org/10.1104/pp.110.155119	journal	May 2010
Bacterial catabolism of lignin-derived aromatics: New findings in a recent decade: Update on bacterial lignin catabolism: Bacterial catabolism of lignin-derived aromatics Kamimura, Naofumi; Takahashi, Kenji; Mori, Kosuke Environmental Microbiology Reports, Vol. 9, Issue 6 https://doi.org/10.1111/1758-2229.12597	journal	November 2017
Chiral Alcohols by Enantioselective Enzymatic Oxidation Hummel, W.; Riebel, B. Annals of the New York Academy of Sciences, Vol. 799, Issue 1 Enzyme Engine https://doi.org/10.1111/j.1749-6632.1996.tb33279.x	journal	October 1996
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
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
Cumate-Inducible Gene Expression System for Sphingomonads and Other Alphaproteobacteria Kaczmarczyk, Andreas; Vorholt, Julia A.; Francez-Charlot, Anne Applied and Environmental Microbiology, Vol. 79, Issue 21 https://doi.org/10.1128/AEM.02296-13	journal	November 2013
Markerless Gene Deletion System for Sphingomonads Kaczmarczyk, Andreas; Vorholt, Julia A.; Francez-Charlot, Anne Applied and Environmental Microbiology, Vol. 78, Issue 10 https://doi.org/10.1128/AEM.07347-11	journal	March 2012
Complete Genome Sequence of Sphingobium sp. Strain SYK-6, a Degrader of Lignin-Derived Biaryls and Monoaryls Masai, E.; Kamimura, N.; Kasai, D. Journal of Bacteriology, Vol. 194, Issue 2 https://doi.org/10.1128/JB.06254-11	journal	December 2011
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
Initial reactions involved in the dissimilation of mandelate by Rhodotorula graminis Durham, D. R. Journal of Bacteriology, Vol. 160, Issue 2 https://doi.org/10.1128/jb.160.2.778-780.1984	journal	November 1984
Structural and Enzymatical Comparison of Lignostilbene- α,β -dioxygenase Isozymes, I, II, and III, from Pseudomonas paucimobilis TMY1009 Kamoda, Shigehiro; Saburi, Yoshimasa Bioscience, Biotechnology, and Biochemistry, Vol. 57, Issue 6 https://doi.org/10.1271/bbb.57.931	journal	January 1993
Cloning of a Lignostilbene-α,β-dioxygenase Isozyme Gene fromPseudomonas paucimohilisTMY1009 Kamoda, Shigehiro; Saburi, Yoshimasa Bioscience, Biotechnology, and Biochemistry, Vol. 59, Issue 10 https://doi.org/10.1271/bbb.59.1866	journal	January 1995
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
Purification and some properties of two C.ALPHA.-dehydrogenases oxidizing dimeric lignin model compounds from Pseudomonas sp. TMY1009. Habu, Naoto; Samejima, Masahiro; Saburi, Yoshimasa Agricultural and Biological Chemistry, Vol. 52, Issue 12 https://doi.org/10.1271/bbb1961.52.3073	journal	January 1988
Purification and some properties of lignostilbene-.ALPHA.,.BETA.-dioxygenase responsible for the C.ALPHA.-C.BETA. cleavage of a diarylpropane type lignin model compound from Pseudomonas sp. TMY1009. Kamoda, Shigehiro; Habu, Naoto; Samejima, Masahiro Agricultural and Biological Chemistry, Vol. 53, Issue 10 https://doi.org/10.1271/bbb1961.53.2757	journal	January 1989
Purification and some properties of the enzyme catalyzing the C.GAMMA.-elimination of a diarylpropane-type lignin model from Pseudomonas paucimobilis TMY1009. Kishi, Katsuyuki; Habu, Naoto; Samejima, Masahiro Agricultural and Biological Chemistry, Vol. 55, Issue 5 https://doi.org/10.1271/bbb1961.55.1319	journal	January 1991
Synthesis of 1,2-Diarylpropane-1,3-Diols and Determination of their Configurations Nakatsubo, Fumiaki; Higuchi, Takayoshi Holzforschung, Vol. 29, Issue 6 https://doi.org/10.1515/hfsg.1975.29.6.193	journal	January 1975
Oligomeric interactions maintain active‐site structure in a noncooperative enzyme family Li, Yaohui; Zhang, Rongzhen; Wang, Chi The EMBO Journal, Vol. 41, Issue 17 https://doi.org/10.15252/embj.2021108368	journal	July 2022

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Title: Stereoinversion via Alcohol Dehydrogenases Enables Complete Catabolism of β-1-Type Lignin-Derived Aromatic Isomers

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