Response of Pseudomonas putida to Complex, Aromatic-Rich Fractions from Biomass
Abstract
There is strong interest in the valorization of lignin to produce valuable products; however, its structural complexity has been a conversion bottleneck. Chemical pretreatment liberates lignin-derived soluble fractions that may be upgraded by bioconversion. Here, cholinium ionic liquid pretreatment of sorghum produced soluble, aromatic-rich fractions that were converted by Pseudomonas putida (P. putida), a promising host for aromatic bioconversion. Growth studies and mutational analysis demonstrated that P. putida growth on these fractions was dependent on aromatic monomers but unknown factors also contributed. Proteomic and metabolomic analyses indicated that these unknown factors were amino acids and residual ionic liquid; the oligomeric aromatic fraction derived from lignin was not converted. A cholinium catabolic pathway was identified, and the deletion of the pathway stopped the ability of P. putida to grow on cholinium ionic liquid. This work demonstrates that aromatic-rich fractions obtained through pretreatment contain multiple substrates; conversion strategies should account for this complexity.
- Authors:
-
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst. and Biological Systems and Engineering Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst.
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Institute and Biological Systems and Engineering Division
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst.; Sandia National Lab. (SNL-CA), Livermore, CA (United States). Biomass Science and Conversion Technology
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst. and Molecular Biophysics and Integrated Bioimaging Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Joint BioEnergy Inst. and Biological Systems and Engineering Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering and Dept. of Chemical & Biomolecular Engineering,; Danish Technical Univ.,Lyngby (Denmark). Center for Biosustainability; Shenzhen Inst. for Advanced Technology (China). Inst. for Synthetic Biology, Center for Synthetic Biochemistry
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1633268
- Alternate Identifier(s):
- OSTI ID: 1616632
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- ChemSusChem
- Additional Journal Information:
- Journal Volume: 13; Journal Issue: 17; Journal ID: ISSN 1864-5631
- Publisher:
- ChemPubSoc Europe
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 09 BIOMASS FUELS; biomass; biotransformations; enzymes; ionic liquids; proteomics; base-catalyzed depolymerization; lignin-derived aromatic monomer; lignin valorization
Citation Formats
Park, Mee‐Rye, Chen, Yan, Thompson, Mitchell, Benites, Veronica T., Fong, Bonnie, Petzold, Christopher J., Baidoo, Edward E. K., Gladden, John M., Adams, Paul D., Keasling, Jay D., Simmons, Blake A., and Singer, Steven W. Response of Pseudomonas putida to Complex, Aromatic-Rich Fractions from Biomass. United States: N. p., 2020.
Web. doi:10.1002/cssc.202000268.
Park, Mee‐Rye, Chen, Yan, Thompson, Mitchell, Benites, Veronica T., Fong, Bonnie, Petzold, Christopher J., Baidoo, Edward E. K., Gladden, John M., Adams, Paul D., Keasling, Jay D., Simmons, Blake A., & Singer, Steven W. Response of Pseudomonas putida to Complex, Aromatic-Rich Fractions from Biomass. United States. https://doi.org/10.1002/cssc.202000268
Park, Mee‐Rye, Chen, Yan, Thompson, Mitchell, Benites, Veronica T., Fong, Bonnie, Petzold, Christopher J., Baidoo, Edward E. K., Gladden, John M., Adams, Paul D., Keasling, Jay D., Simmons, Blake A., and Singer, Steven W. Wed .
"Response of Pseudomonas putida to Complex, Aromatic-Rich Fractions from Biomass". United States. https://doi.org/10.1002/cssc.202000268. https://www.osti.gov/servlets/purl/1633268.
@article{osti_1633268,
title = {Response of Pseudomonas putida to Complex, Aromatic-Rich Fractions from Biomass},
author = {Park, Mee‐Rye and Chen, Yan and Thompson, Mitchell and Benites, Veronica T. and Fong, Bonnie and Petzold, Christopher J. and Baidoo, Edward E. K. and Gladden, John M. and Adams, Paul D. and Keasling, Jay D. and Simmons, Blake A. and Singer, Steven W.},
abstractNote = {There is strong interest in the valorization of lignin to produce valuable products; however, its structural complexity has been a conversion bottleneck. Chemical pretreatment liberates lignin-derived soluble fractions that may be upgraded by bioconversion. Here, cholinium ionic liquid pretreatment of sorghum produced soluble, aromatic-rich fractions that were converted by Pseudomonas putida (P. putida), a promising host for aromatic bioconversion. Growth studies and mutational analysis demonstrated that P. putida growth on these fractions was dependent on aromatic monomers but unknown factors also contributed. Proteomic and metabolomic analyses indicated that these unknown factors were amino acids and residual ionic liquid; the oligomeric aromatic fraction derived from lignin was not converted. A cholinium catabolic pathway was identified, and the deletion of the pathway stopped the ability of P. putida to grow on cholinium ionic liquid. This work demonstrates that aromatic-rich fractions obtained through pretreatment contain multiple substrates; conversion strategies should account for this complexity.},
doi = {10.1002/cssc.202000268},
journal = {ChemSusChem},
number = 17,
volume = 13,
place = {United States},
year = {2020},
month = {3}
}
Web of Science
Works referenced in this record:
Polyesters of 2-Pyrone-4,6-Dicarboxylic Acid (PDC) Obtained from a Metabolic Intermediate of Lignin
journal, November 2007
- Michinobu, Tsuyoshi; Hishida, Masakiyo; Sato, Masae
- Polymer Journal, Vol. 40, Issue 1
Saccharomyces cerevisiae-Based Molecular Tool Kit for Manipulation of Genes from Gram-Negative Bacteria
journal, July 2006
- Shanks, Robert; Caiazza, Nicky; Hinsa, Shannon
- Applied and Environmental Microbiology, Vol. 72, Issue 7, p. 5027-5036
Room-Temperature Ionic Liquids: Solvents for Synthesis and Catalysis. 2
journal, May 2011
- Hallett, Jason P.; Welton, Tom
- Chemical Reviews, Vol. 111, Issue 5
Standard Flow Liquid Chromatography for Shotgun Proteomics in Bioenergy Research
journal, April 2015
- González Fernández-Niño, Susana M.; Smith-Moritz, A. Michelle; Chan, Leanne Jade G.
- Frontiers in Bioengineering and Biotechnology, Vol. 3
Metabolic engineering of Pseudomonas putida for increased polyhydroxyalkanoate production from lignin
journal, January 2020
- Salvachúa, Davinia; Rydzak, Thomas; Auwae, Raquel
- Microbial Biotechnology, Vol. 13, Issue 1
Production of poly(3-hydroxybutyrate-co-3-hydroxyvalerate) P(3HB-co-3HV) with a broad range of 3HV content at high yields by Burkholderia sacchari IPT 189
journal, July 2007
- Rocha, Rafael C. S.; da Silva, Luiziana F.; Taciro, Marilda K.
- World Journal of Microbiology and Biotechnology, Vol. 24, Issue 3
Microbial utilization and biopolyester synthesis of bagasse hydrolysates
journal, November 2008
- Yu, Jian; Stahl, Heiko
- Bioresource Technology, Vol. 99, Issue 17
Structural Analysis of Wheat Straw Lignin by Quantitative 31 P and 2D NMR Spectroscopy. The Occurrence of Ester Bonds and α-O-4 Substructures
journal, April 1997
- Crestini, Claudia; Argyropoulos, Dimitris S.
- Journal of Agricultural and Food Chemistry, Vol. 45, Issue 4
Towards lignin consolidated bioprocessing: simultaneous lignin depolymerization and product generation by bacteria
journal, January 2015
- Salvachúa, Davinia; Karp, Eric M.; Nimlos, Claire T.
- Green Chemistry, Vol. 17, Issue 11
j5 DNA Assembly Design Automation Software
journal, December 2011
- Hillson, Nathan J.; Rosengarten, Rafael D.; Keasling, Jay D.
- ACS Synthetic Biology, Vol. 1, Issue 1, p. 14-21
Homeostasis and Catabolism of Choline and Glycine Betaine: Lessons from Pseudomonas aeruginosa
journal, January 2013
- Wargo, Matthew J.
- Applied and Environmental Microbiology, Vol. 79, Issue 7
Evaluation of two autoinducer-2 quantification methods for application in marine environments
journal, March 2018
- Wang, T. -N.; Kaksonen, A. H.; Hong, P. -Y.
- Journal of Applied Microbiology, Vol. 124, Issue 6
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production
journal, February 2007
- Himmel, M. E.; Ding, S.-Y.; Johnson, D. K.
- Science, Vol. 315, Issue 5813, p. 804-807
Peroxidase-dependent cross-linking reactions of p-hydroxycinnamates in plant cell walls
journal, January 2004
- Ralph, John; Bunzel, Mirko; Marita, Jane M.
- Phytochemistry Reviews, Vol. 3, Issue 1-2, p. 79-96
Protein content and amino acid composition of some varieties of grain sorghum
journal, March 1968
- Virupaksha, T. K.; Sastry, L. V. S.
- Journal of Agricultural and Food Chemistry, Vol. 16, Issue 2
Purification and characterization of isocitrate lyase fromEscherichia coli
journal, November 1986
- Robertson, Eugene F.; Reeves, Henry C.
- Current Microbiology, Vol. 14, Issue 6
Lignin valorization through integrated biological funneling and chemical catalysis
journal, August 2014
- Linger, J. G.; Vardon, D. R.; Guarnieri, M. T.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 33, p. 12013-12018
Kinetic understanding of nitrogen supply condition on biosynthesis of polyhydroxyalkanoate from benzoate by Pseudomonas putida KT2440
journal, February 2019
- Xu, Zhangyang; Li, Xiaolu; Hao, Naijia
- Bioresource Technology, Vol. 273
Comparison of alkali treatments for efficient release of p-coumaric acid and enzymatic saccharification of sorghum pith
journal, May 2016
- Jiang, Kankan; Li, Lulu; Long, Liangkun
- Bioresource Technology, Vol. 207
The role of isocitrate lyase and the glyoxylate cycle in Escherichia coli growing under glucose limitation
journal, March 2005
- Prasad Maharjan, Ram; Yu, Pak-Lam; Seeto, Shona
- Research in Microbiology, Vol. 156, Issue 2
Enzymatic assembly of DNA molecules up to several hundred kilobases
journal, April 2009
- Gibson, Daniel G.; Young, Lei; Chuang, Ray-Yuan
- Nature Methods, Vol. 6, Issue 5, p. 343-345
Eliminating a global regulator of carbon catabolite repression enhances the conversion of aromatic lignin monomers to muconate in Pseudomonas putida KT2440
journal, December 2017
- Johnson, Christopher W.; Abraham, Paul E.; Linger, Jeffrey G.
- Metabolic Engineering Communications, Vol. 5
Structural Characterization of Wheat Straw Lignin as Revealed by Analytical Pyrolysis, 2D-NMR, and Reductive Cleavage Methods
journal, December 2011
- del Río, José C.; Rencoret, Jorge; Prinsen, Pepijn
- Journal of Agricultural and Food Chemistry, Vol. 60, Issue 23
Lignin to lipid bioconversion by oleaginous Rhodococci
journal, January 2013
- Kosa, Matyas; Ragauskas, Arthur J.
- Green Chemistry, Vol. 15, Issue 8
Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440
journal, December 2002
- Jimenez, Jose Ignacio; Minambres, Baltasar; Garcia, Jose Luis
- Environmental Microbiology, Vol. 4, Issue 12, p. 824-841
Lignin Valorization: Improving Lignin Processing in the Biorefinery
journal, May 2014
- Ragauskas, A. J.; Beckham, G. T.; Biddy, M. J.
- Science, Vol. 344, Issue 6185, p. 1246843-1246843
The effects of model aromatic lignin compounds on growth and lipid accumulation of Rhodococcus rhodochrous
journal, July 2017
- Shields-Menard, Sara A.; AmirSadeghi, Marta; Green, Magan
- International Biodeterioration & Biodegradation, Vol. 121
Conversion of lignin model compounds by Pseudomonas putida KT2440 and isolates from compost
journal, March 2017
- Ravi, Krithika; García-Hidalgo, Javier; Gorwa-Grauslund, Marie F.
- Applied Microbiology and Biotechnology, Vol. 101, Issue 12
Sequential fractionation of the lignocellulosic components in hardwood based on steam explosion and hydrotropic extraction
journal, January 2019
- Olsson, Johanna; Novy, Vera; Nielsen, Fredrik
- Biotechnology for Biofuels, Vol. 12, Issue 1
Organosolv lignin depolymerization with different base catalysts
journal, April 2012
- Toledano, Ana; Serrano, Luis; Labidi, Jalel
- Journal of Chemical Technology & Biotechnology, Vol. 87, Issue 11
Hydrogenolysis of biorefinery corncob lignin into aromatic phenols over activated carbon-supported nickel
journal, January 2019
- Wang, Shuizhong; Gao, Wa; Xiao, Ling-Ping
- Sustainable Energy & Fuels, Vol. 3, Issue 2
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
Directed bioconversion of Kraft lignin to polyhydroxyalkanoate by Cupriavidus basilensis B-8 without any pretreatment
journal, January 2017
- Shi, Yan; Yan, Xu; Li, Qiang
- Process Biochemistry, Vol. 52
Ferulic acid: a key component in grass lignocellulose recalcitrance to hydrolysis
journal, November 2014
- de Oliveira, Dyoni Matias; Finger-Teixeira, Aline; Rodrigues Mota, Thatiane
- Plant Biotechnology Journal, Vol. 13, Issue 9
Construction ofpha-Operon-Defined Knockout Mutants ofPseudomonas putida KT2442 and their Applications in Poly(hydroxyalkanoate) Production
journal, February 2007
- Ouyang, Shao-Ping; Liu, Qian; Fang, Lei
- Macromolecular Bioscience, Vol. 7, Issue 2
Whole plant cell wall characterization using solution-state 2D NMR
journal, August 2012
- Mansfield, Shawn D.; Kim, Hoon; Lu, Fachuang
- Nature Protocols, Vol. 7, Issue 9
Acetate scavenging activity in Escherichia coli: interplay of acetyl–CoA synthetase and the PEP–glyoxylate cycle in chemostat cultures
journal, September 2011
- Renilla, Sergio; Bernal, Vicente; Fuhrer, Tobias
- Applied Microbiology and Biotechnology, Vol. 93, Issue 5
HipA-Triggered Growth Arrest and β-Lactam Tolerance in Escherichia coli Are Mediated by RelA-Dependent ppGpp Synthesis
journal, May 2013
- Bokinsky, G.; Baidoo, E. E. K.; Akella, S.
- Journal of Bacteriology, Vol. 195, Issue 14, p. 3173-3182
2016 update of the PRIDE database and its related tools
journal, November 2015
- Vizcaíno, Juan Antonio; Csordas, Attila; del-Toro, Noemi
- Nucleic Acids Research, Vol. 44, Issue D1
Base-Catalyzed Depolymerization of Biorefinery Lignins
journal, December 2015
- Katahira, Rui; Mittal, Ashutosh; McKinney, Kellene
- ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 3
Identification of Two Gene Clusters and a Transcriptional Regulator Required for Pseudomonas aeruginosa Glycine Betaine Catabolism
journal, October 2007
- Wargo, M. J.; Szwergold, B. S.; Hogan, D. A.
- Journal of Bacteriology, Vol. 190, Issue 8
The Catalytic Valorization of Lignin for the Production of Renewable Chemicals
journal, June 2010
- Zakzeski, Joseph; Bruijnincx, Pieter C. A.; Jongerius, Anna L.
- Chemical Reviews, Vol. 110, Issue 6, p. 3552-3599
Adipic acid production from lignin
journal, January 2015
- Vardon, Derek R.; Franden, Mary Ann; Johnson, Christopher W.
- Energy & Environmental Science, Vol. 8, Issue 2
Production of hydroxycinnamoyl anthranilates from glucose in Escherichia coli
journal, January 2013
- Eudes, Aymerick; Juminaga, Darmawi; Baidoo, Edward E. K.
- Microbial Cell Factories, Vol. 12, Issue 1
Pseudomonas putida as a functional chassis for industrial biocatalysis: From native biochemistry to trans-metabolism
journal, November 2018
- Nikel, Pablo I.; de Lorenzo, Víctor
- Metabolic Engineering, Vol. 50
Across the Board: Mark Mascal on the Challenges of Lignin Biorefining
journal, December 2019
- Mascal, Mark
- ChemSusChem, Vol. 13, Issue 1
Lignocellulosic biomass: a sustainable platform for the production of bio-based chemicals and polymers
journal, January 2015
- Isikgor, Furkan H.; Becer, C. Remzi
- Polymer Chemistry, Vol. 6, Issue 25
Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5
journal, January 2010
- Kim, Hoon; Ralph, John
- Org. Biomol. Chem., Vol. 8, Issue 3
Aromatic Monomers by in Situ Conversion of Reactive Intermediates in the Acid-Catalyzed Depolymerization of Lignin
journal, June 2015
- Deuss, Peter J.; Scott, Martin; Tran, Fanny
- Journal of the American Chemical Society, Vol. 137, Issue 23
Succinate-mediated catabolite repression control on the production of glycine betaine catabolic enzymes in Pseudomonas aeruginosa PAO1 under low and elevated salinities
journal, May 2006
- Diab, F.
- Microbiology, Vol. 152, Issue 5
DeviceEditor visual biological CAD canvas
journal, December 2012
- Chen, Joanna; Densmore, Douglas; Ham, Timothy S.
- Journal of Biological Engineering, Vol. 6, Issue 1
One-pot integrated biofuel production using low-cost biocompatible protic ionic liquids
journal, January 2017
- Sun, Jian; Konda, N. V. S. N. Murthy; Parthasarathi, Ramakrishnan
- Green Chemistry, Vol. 19, Issue 13
Characterization of nonderivatized plant cell walls using high-resolution solution-state NMR spectroscopy
journal, June 2008
- Yelle, Daniel J.; Ralph, John; Frihart, Charles R.
- Magnetic Resonance in Chemistry, Vol. 46, Issue 6
Impact of lignin polymer backbone esters on ionic liquid pretreatment of poplar
journal, April 2017
- Kim, Kwang Ho; Dutta, Tanmoy; Ralph, John
- Biotechnology for Biofuels, Vol. 10, Issue 1
Pathway of p-Coumaric Acid Incorporation into Maize Lignin As Revealed by NMR
journal, October 1994
- Ralph, John; Hatfield, Ronald D.; Quideau, Stephane
- Journal of the American Chemical Society, Vol. 116, Issue 21, p. 9448-9456
Hydrothermal Liquefaction of Enzymatic Hydrolysis Lignin: Biomass Pretreatment Severity Affects Lignin Valorization
journal, March 2018
- Jensen, Mads M.; Djajadi, Demi T.; Torri, Cristian
- ACS Sustainable Chemistry & Engineering, Vol. 6, Issue 5
Lignin depolymerisation strategies: towards valuable chemicals and fuels
journal, January 2014
- Xu, Chunping; Arancon, Rick Arneil D.; Labidi, Jalel
- Chemical Society Reviews, Vol. 43, Issue 22, p. 7485-7500
Composition of non-woody plant lignins and cinnamic acids by Py-GC/MS, Py/TMAH and FT-IR
journal, May 2007
- del Río, José C.; Gutiérrez, Ana; Rodríguez, Isabel M.
- Journal of Analytical and Applied Pyrolysis, Vol. 79, Issue 1-2
Design of a dynamic sensor-regulator system for production of chemicals and fuels derived from fatty acids
journal, March 2012
- Zhang, Fuzhong; Carothers, James M.; Keasling, Jay D.
- Nature Biotechnology, Vol. 30, Issue 4
One-pot ionic liquid pretreatment and saccharification of switchgrass
journal, January 2013
- Shi, Jian; Gladden, John M.; Sathitsuksanoh, Noppadon
- Green Chemistry, Vol. 15, Issue 9
Screening of Marine Bacteria To Synthesize Polyhydroxyalkanoate from Lignin: Contribution of Lignin Derivatives to Biosynthesis by Oceanimonas doudoroffii
journal, February 2015
- Numata, Keiji; Morisaki, Kumiko
- ACS Sustainable Chemistry & Engineering, Vol. 3, Issue 4
Hydroxycinnamates in lignification
journal, August 2009
- Ralph, John
- Phytochemistry Reviews, Vol. 9, Issue 1, p. 65-83
Base-Catalyzed Depolymerization of Solid Lignin-Rich Streams Enables Microbial Conversion
journal, August 2017
- Rodriguez, Alberto; Salvachúa, Davinia; Katahira, Rui
- ACS Sustainable Chemistry & Engineering, Vol. 5, Issue 9
The revisited genome of Pseudomonas putida KT2440 enlightens its value as a robust metabolic chassis : Re-annotation of the Pseudomonas putida KT2440 genome
journal, April 2016
- Belda, Eugeni; van Heck, Ruben G. A.; José Lopez-Sanchez, Maria
- Environmental Microbiology, Vol. 18, Issue 10
Demonstrating a separation-free process coupling ionic liquid pretreatment, saccharification, and fermentation with Rhodosporidium toruloides to produce advanced biofuels
journal, January 2018
- Sundstrom, Eric; Yaegashi, Junko; Yan, Jipeng
- Green Chemistry, Vol. 20, Issue 12
Monolignol acylation and lignin structure in some nonwoody plants: A 2D NMR study
journal, November 2008
- Martínez, Ángel T.; Rencoret, Jorge; Marques, Gisela
- Phytochemistry, Vol. 69, Issue 16, p. 2831-2843
Transition metal (Ti, Mo, Nb, W) nitride catalysts for lignin depolymerisation
journal, January 2016
- Chen, Long; Korányi, Tamás I.; Hensen, Emiel J. M.
- Chemical Communications, Vol. 52, Issue 60
mini-Tn7 insertion in bacteria with single attTn7 sites: example Pseudomonas aeruginosa
journal, June 2006
- Choi, Kyoung-Hee; Schweizer, Herbert P.
- Nature Protocols, Vol. 1, Issue 1
Efficient dehydration and recovery of ionic liquid after lignocellulosic processing using pervaporation
journal, June 2017
- Sun, Jian; Shi, Jian; Murthy Konda, N. V. S. N.
- Biotechnology for Biofuels, Vol. 10, Issue 1
Quantitative release of fatty acids from lipids by a simple hydrolysis procedure.
journal, August 1983
- Aveldaño, M. I.; Horrocks, L. A.
- Journal of Lipid Research, Vol. 24, Issue 8