Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization

Varman, Arul M.; He, Lian; Follenfant, Rhiannon; Wu, Weihua; Wemmer, Sarah; Wrobel, Steven A.; Tang, Yinjie J.; Singh, Seema

doi:10.1073/pnas.1606043113

Title: Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization

Journal Article · Thu Sep 15 00:00:00 EDT 2016 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.1606043113· OSTI ID:1325317

Varman, Arul M. ^[1]; He, Lian ^[2]; Follenfant, Rhiannon ^[1]; Wu, Weihua ^[1]; Wemmer, Sarah ^[1]; Wrobel, Steven A. ^[1]; Tang, Yinjie J. ^[2]; Singh, Seema ^[3]

Biomass Science and Conversion Technology Department, Sandia National Laboratories, Livermore, CA 94550,
Department of Energy, Environmental and Chemical Engineering, Washington University in St. Louis, St. Louis, MO 63130,
Biomass Science and Conversion Technology Department, Sandia National Laboratories, Livermore, CA 94550,, Department of Bioproducts and Biosystems Engineering, University of Minnesota, St. Paul, MN 55108

Lignin is a major resources for the production of next generation renewable aromatics. Sphingobium sp. SYK-6 is a bacterium that has been well-studied for the breakdown of lignin-derived compounds. There has been a lot of interest in SYK-6 lignolytic activity and many recent works have focused on understanding the unique catabolic pathway it possesses for the degradation of lignin derived monomers and oligomers. Furthermore, there has been no prior effort in understanding the central fluxome based on lignin derived substrates into value-added chemicals.

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Research Organization:: Sandia National Lab. (SNL-CA), Livermore, CA (United States)

Sponsoring Organization:: USDOE National Nuclear Security Administration (NNSA)

Grant/Contract Number:: 16-0758; AC04-94AL85000

OSTI ID:: 1325317

Alternate ID(s):: OSTI ID: 1239396

Report Number(s):: SAND-2016-0538J

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Vol. 113 Journal Issue: 40; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 64 works

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References (56)

Survey of renewable chemicals produced from lignocellulosic biomass during ionic liquid pretreatment Varanasi, Patanjali; Singh, Priyanka; Auer, Manfred Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-14	journal	January 2013
Lignin modification improves fermentable sugar yields for biofuel production Chen, Fang; Dixon, Richard A. Nature Biotechnology, Vol. 25, Issue 7, p. 759-761 https://doi.org/10.1038/nbt1316	journal	June 2007
Incomplete Wood-Ljungdahl pathway facilitates one-carbon metabolism in organohalide-respiring Dehalococcoides mccartyi Zhuang, W. -Q.; Yi, S.; Bill, M. Proceedings of the National Academy of Sciences, Vol. 111, Issue 17 https://doi.org/10.1073/pnas.1321542111	journal	April 2014
Tetrahydrofolate-dependent vanillate and syringateO-demethylation links tightly to one-carbon metabolic pathway associated with amino acid synthesis and DNA methylation in the lignin metabolism ofSphingomonas paucimobilis SYK-6 Sonoki, Tomonori; Otsuka, Yuichiro; Ikeda, Seiichiro Journal of Wood Science, Vol. 48, Issue 5 https://doi.org/10.1007/BF00770706	journal	October 2002
Characterization of ligV Essential for Catabolism of Vanillin by Sphingomonas paucimobilis SYK-6 Masai, Eiji; Yamamoto, Yuko; Inoue, Tomohiko Bioscience, Biotechnology, and Biochemistry, Vol. 71, Issue 10 https://doi.org/10.1271/bbb.70267	journal	October 2007
Central metabolic responses to the overproduction of fatty acids in Escherichia coli based on ¹³ C-metabolic flux analysis He, Lian; Xiao, Yi; Gebreselassie, Nikodimos Biotechnology and Bioengineering, Vol. 111, Issue 3 https://doi.org/10.1002/bit.25124	journal	October 2013
Isolation and characterization of novel bacterial strains exhibiting ligninolytic potential Bandounas, Luaine; Wierckx, Nick JP; de Winde, Johannes H. BMC Biotechnology, Vol. 11, Issue 1 https://doi.org/10.1186/1472-6750-11-94	journal	January 2011
Catalytic Lignin Valorization Process for the Production of Aromatic Chemicals and Hydrogen Zakzeski, Joseph; Jongerius, Anna L.; Bruijnincx, Pieter C. A. ChemSusChem, Vol. 5, Issue 8 https://doi.org/10.1002/cssc.201100699	journal	June 2012
Efficient biomass pretreatment using ionic liquids derived from lignin and hemicellulose Socha, A. M.; Parthasarathi, R.; Shi, J. Proceedings of the National Academy of Sciences, Vol. 111, Issue 35 https://doi.org/10.1073/pnas.1405685111	journal	August 2014
From zero to hero—Design-based systems metabolic engineering of Corynebacterium glutamicum for l-lysine production Becker, Judith; Zelder, Oskar; Häfner, Stefan Metabolic Engineering, Vol. 13, Issue 2 https://doi.org/10.1016/j.ymben.2011.01.003	journal	March 2011
Bidirectional reaction steps in metabolic networks: II. Flux estimation and statistical analysis Wiechert, Wolfgang; Siefke, Claudia; de Graaf, Albert A. Biotechnology and Bioengineering, Vol. 55, Issue 1 https://doi.org/10.1002/(SICI)1097-0290(19970705)55:1<118::AID-BIT13>3.0.CO;2-I	journal	July 1997
Parallel labeling experiments validate Clostridium acetobutylicum metabolic network model for 13C metabolic flux analysis Au, Jennifer; Choi, Jungik; Jones, Shawn W. Metabolic Engineering, Vol. 26 https://doi.org/10.1016/j.ymben.2014.08.002	journal	November 2014
Metabolic Flux Analysis of the Mixotrophic Metabolisms in the Green Sulfur Bacterium Chlorobaculum tepidum Feng, Xueyang; Tang, Kuo-Hsiang; Blankenship, Robert E. Journal of Biological Chemistry, Vol. 285, Issue 50, p. 39544-39550 https://doi.org/10.1074/jbc.M110.162958	journal	October 2010
The Secret Life of NAD ⁺ : An Old Metabolite Controlling New Metabolic Signaling Pathways Houtkooper, Riekelt H.; Cantó, Carles; Wanders, Ronald J. Endocrine Reviews, Vol. 31, Issue 2 https://doi.org/10.1210/er.2009-0026	journal	April 2010
Technology for conversion of lignocellulosic biomass to ethanol Szczodrak, Janusz; Fiedurek, Jan Biomass and Bioenergy, Vol. 10, Issue 5-6 https://doi.org/10.1016/0961-9534(95)00114-X	journal	January 1996
Lignin valorization through integrated biological funneling and chemical catalysis Linger, J. G.; Vardon, D. R.; Guarnieri, M. T. Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018 https://doi.org/10.1073/pnas.1410657111	journal	August 2014
Evidence supporting dissimilatory and assimilatory lignin degradation in Enterobacter lignolyticus SCF1 DeAngelis, Kristen M.; Sharma, Deepak; Varney, Rebecca Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00280	journal	January 2013
From Gene Towards Selective Biomass Valorization: Bacterial β-Etherases with Catalytic Activity on Lignin-Like Polymers Picart, Pere; Müller, Christoph; Mottweiler, Jakob ChemSusChem, Vol. 7, Issue 11 https://doi.org/10.1002/cssc.201402465	journal	September 2014
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
Metabolic engineering of Escherichia coli for direct production of 1,4-butanediol Yim, Harry; Haselbeck, Robert; Niu, Wei Nature Chemical Biology, Vol. 7, Issue 7 https://doi.org/10.1038/nchembio.580	journal	May 2011
Elucidation of intrinsic biosynthesis yields using 13C-based metabolism analysis Varman, Arul M.; He, Lian; You, Le Microbial Cell Factories, Vol. 13, Issue 1 https://doi.org/10.1186/1475-2859-13-42	journal	January 2014
The Role of Pyruvate Ferredoxin Oxidoreductase in Pyruvate Synthesis during Autotrophic Growth by the Wood-Ljungdahl Pathway Furdui, Cristina; Ragsdale, Stephen W. Journal of Biological Chemistry, Vol. 275, Issue 37 https://doi.org/10.1074/jbc.M003291200	journal	June 2000
Ribose-5-Phosphate Biosynthesis in Methanocaldococcus jannaschii Occurs in the Absence of a Pentose-Phosphate Pathway Grochowski, L. L.; Xu, H.; White, R. H. Journal of Bacteriology, Vol. 187, Issue 21 https://doi.org/10.1128/JB.187.21.7382-7389.2005	journal	October 2005
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
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
Exploring bacterial lignin degradation Brown, Margaret E.; Chang, Michelle CY Current Opinion in Chemical Biology, Vol. 19 https://doi.org/10.1016/j.cbpa.2013.11.015	journal	April 2014
Valorization of Biomass: Deriving More Value from Waste Tuck, C. O.; Perez, E.; Horvath, I. T. Science, Vol. 337, Issue 6095, p. 695-699 https://doi.org/10.1126/science.1218930	journal	August 2012
Pathways for degradation of lignin in bacteria and fungi Bugg, Timothy D. H.; Ahmad, Mark; Hardiman, Elizabeth M. Natural Product Reports, Vol. 28, Issue 12, p. 1883-1896 https://doi.org/10.1039/c1np00042j	journal	January 2011
Loosening lignin's grip on biofuel production Chapple, Clint; Ladisch, Michael; Meilan, Rick Nature Biotechnology, Vol. 25, Issue 7, p. 746-748 https://doi.org/10.1038/nbt0707-746	journal	July 2007
Formic-acid-induced depolymerization of oxidized lignin to aromatics Rahimi, Alireza; Ulbrich, Arne; Coon, Joshua J. Nature, Vol. 515, Issue 7526, p. 249-252 https://doi.org/10.1038/nature13867	journal	November 2014
O-Demethylase from Acetobacterium dehalogenans . Substrate specificity and function of the participating proteins Kaufmann, Franz; Wohlfarth, Gert; Diekert, Gabriele European Journal of Biochemistry, Vol. 253, Issue 3 https://doi.org/10.1046/j.1432-1327.1998.2530706.x	journal	May 1998
Genetic and Biochemical Characterization of 4-Carboxy-2-Hydroxymuconate-6-Semialdehyde Dehydrogenase and Its Role in the Protocatechuate 4,5-Cleavage Pathway in Sphingomonas paucimobilis SYK-6 Masai, E.; Momose, K.; Hara, H. Journal of Bacteriology, Vol. 182, Issue 23 https://doi.org/10.1128/JB.182.23.6651-6658.2000	journal	December 2000
13C metabolic flux analysis of the extremely thermophilic, fast growing, xylose-utilizing Geobacillus strain LC300 Cordova, Lauren T.; Antoniewicz, Maciek R. Metabolic Engineering, Vol. 33 https://doi.org/10.1016/j.ymben.2015.06.004	journal	January 2016
Metabolic flux analysis of Escherichia coli K12 grown on 13C-labeled acetate and glucose using GC-MS and powerful flux calculation method Zhao, Jiao; Shimizu, Kazuyuki Journal of Biotechnology, Vol. 101, Issue 2 https://doi.org/10.1016/S0168-1656(02)00316-4	journal	March 2003
Metabolic flux analysis of CHO cells in perfusion culture by metabolite balancing and 2D [13C, 1H] COSY NMR spectroscopy Goudar, Chetan; Biener, Richard; Boisart, C. Metabolic Engineering, Vol. 12, Issue 2 https://doi.org/10.1016/j.ymben.2009.10.007	journal	March 2010
Elementary metabolite units (EMU): A novel framework for modeling isotopic distributions Antoniewicz, Maciek R.; Kelleher, Joanne K.; Stephanopoulos, Gregory Metabolic Engineering, Vol. 9, Issue 1 https://doi.org/10.1016/j.ymben.2006.09.001	journal	January 2007
Cloning of a Sphingomonas paucimobilis SYK-6 Gene Encoding a Novel Oxygenase That Cleaves Lignin-Related Biphenyl and Characterization of the Enzyme Peng, Xue; Egashira, Takashi; Hanashiro, Kaoru Applied and Environmental Microbiology, Vol. 64, Issue 7 https://doi.org/10.1128/AEM.64.7.2520-2527.1998	journal	July 1998
Photoautotrophic production of D-lactic acid in an engineered cyanobacterium Varman, Arul M.; Yu, Yi; You, Le Microbial Cell Factories, Vol. 12, Issue 1 https://doi.org/10.1186/1475-2859-12-117	journal	January 2013
Cloning and sequencing of Pseudomonas genes encoding vanillate demethylase. Brunel, F.; Davison, J. Journal of Bacteriology, Vol. 170, Issue 10 https://doi.org/10.1128/jb.170.10.4924-4930.1988	journal	October 1988
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
Biomass conversion: Lignin up for break-down Bruijnincx, Pieter C. A.; Weckhuysen, Bert M. Nature Chemistry, Vol. 6, Issue 12, p. 1035-1036 https://doi.org/10.1038/nchem.2120	journal	December 2014
A Novel Tetrahydrofolate-Dependent O-Demethylase Gene Is Essential for Growth of Sphingomonas paucimobilis SYK-6 with Syringate Masai, E.; Sasaki, M.; Minakawa, Y. Journal of Bacteriology, Vol. 186, Issue 9 https://doi.org/10.1128/JB.186.9.2757-2765.2004	journal	April 2004
The NAD ratio redox paradox: why does too much reductive power cause oxidative stress? Teodoro, João Soeiro; Rolo, Anabela Pinto; Palmeira, Carlos Marques Toxicology Mechanisms and Methods, Vol. 23, Issue 5 https://doi.org/10.3109/15376516.2012.759305	journal	January 2013
Lignin depolymerisation strategies: towards valuable chemicals and fuels Xu, Chunping; Arancon, Rick Arneil D.; Labidi, Jalel Chemical Society Reviews, Vol. 43, Issue 22, p. 7485-7500 https://doi.org/10.1039/C4CS00235K	journal	January 2014
Isotopically nonstationary ¹³ C flux analysis of changes in Arabidopsis thaliana leaf metabolism due to high light acclimation Ma, Fangfang; Jazmin, Lara J.; Young, Jamey D. Proceedings of the National Academy of Sciences, Vol. 111, Issue 47 https://doi.org/10.1073/pnas.1319485111	journal	November 2014
Recent advances in mapping environmental microbial metabolisms through ¹³ C isotopic fingerprints Tang, Joseph Kuo-Hsiang; You, Le; Blankenship, Robert E. Journal of The Royal Society Interface, Vol. 9, Issue 76 https://doi.org/10.1098/rsif.2012.0396	journal	June 2012
Direct cellobiose production from cellulose using sextuple beta-glucosidase gene deletion Neurospora crassa mutants Wu, Weihua; Hildebrand, Amanda; Kasuga, Takao Enzyme and Microbial Technology, Vol. 52, Issue 3 https://doi.org/10.1016/j.enzmictec.2012.12.010	journal	March 2013
Monolignol Ferulate Transferase Introduces Chemically Labile Linkages into the Lignin Backbone Wilkerson, C. G.; Mansfield, S. D.; Lu, F. Science, Vol. 344, Issue 6179, p. 90-93 https://doi.org/10.1126/science.1250161	journal	April 2014
Investigating the Regulation of One-carbon Metabolism in Arabidopsis thaliana Li, Rong; Moore, Maya; King, John Plant and Cell Physiology, Vol. 44, Issue 3 https://doi.org/10.1093/pcp/pcg029	journal	March 2003
Monte Carlo sampling can be used to determine the size and shape of the steady-state flux space Wiback, Sharon J.; Famili, Iman; Greenberg, Harvey J. Journal of Theoretical Biology, Vol. 228, Issue 4 https://doi.org/10.1016/j.jtbi.2004.02.006	journal	June 2004
Folate Metabolism and Requirements Bailey, Lynn B.; Gregory, Jesse F. The Journal of Nutrition, Vol. 129, Issue 4 https://doi.org/10.1093/jn/129.4.779	journal	April 1999
Next-generation biomass feedstocks for biofuel production Simmons, Blake A.; Loque, Dominique; Blanch, Harvey W. Genome Biology, Vol. 9, Issue 12 https://doi.org/10.1186/gb-2008-9-12-242	journal	January 2008
A Tetrahydrofolate-Dependent O-Demethylase, LigM, Is Crucial for Catabolism of Vanillate and Syringate in Sphingomonas paucimobilis SYK-6 Abe, T.; Masai, E.; Miyauchi, K. Journal of Bacteriology, Vol. 187, Issue 6, p. 2030-2037 https://doi.org/10.1128/JB.187.6.2030-2037.2005	journal	March 2005
The Key Role of Anaplerosis and Cataplerosis for Citric Acid Cycle Function Owen, Oliver E.; Kalhan, Satish C.; Hanson, Richard W. Journal of Biological Chemistry, Vol. 277, Issue 34 https://doi.org/10.1074/jbc.R200006200	journal	June 2002
New tools for mass isotopomer data evaluation in13C flux analysis: Mass isotope correction, data consistency checking, and precursor relationships Wahl, S. Aljoscha; Dauner, Michael; Wiechert, Wolfgang Biotechnology and Bioengineering, Vol. 85, Issue 3 https://doi.org/10.1002/bit.10909	journal	January 2004
Location and contribution of individual β-glucosidase from Neurospora crassa to total β-glucosidase activity Wu, Weihua; Kasuga, Takao; Xiong, Xiaochao Archives of Microbiology, Vol. 195, Issue 12 https://doi.org/10.1007/s00203-013-0931-5	journal	October 2013

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Title: Decoding how a soil bacterium extracts building blocks and metabolic energy from ligninolysis provides road map for lignin valorization

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