Advanced Chemical Design for Efficient Lignin Bioconversion

Xie, Shangxian; Sun, Qining; Pu, Yunqiao; Lin, Furong; Sun, Su; Wang, Xin; Ragauskas, Arthur J.; Yuan, Joshua S.

doi:10.1021/acssuschemeng.6b02401

Advanced Chemical Design for Efficient Lignin Bioconversion

Journal Article · Wed Dec 21 23:00:00 EST 2016 · ACS Sustainable Chemistry & Engineering

DOI:https://doi.org/10.1021/acssuschemeng.6b02401· OSTI ID:1344299

Xie, Shangxian ^[1]; Sun, Qining ^[2]; Pu, Yunqiao ^[3]; Lin, Furong ^[1]; Sun, Su ^[1]; Wang, Xin ^[1]; ^[4]; ^[1]

Texas A&M University, College Station, TX (United States)
University of Tennessee, Knoxville, TN (United States)
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
University of Tennessee, Knoxville, TN (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Here, lignin depolymerization mainly involves redox reactions relying on the effective electron transfer. Even though electron mediators were previously used for delignification of paper pulp, no study has established a bioprocess to fragment and solubilize the lignin with an effective laccase–mediator system, in particular, for subsequent microbial bioconversion. Efficient lignin depolymerization was achieved by screening proper electron mediators with laccase to attain a nearly 6-fold increase of kraft lignin solubility compared to the control kraft lignin without laccase treatment. Chemical analysis suggested the release of a low molecular weight fraction of kraft lignin into the solution phase. Moreover, NMR analysis revealed that an efficient enzyme–mediator system can promote the lignin degradation. More importantly, the fundamental mechanisms guided the development of an efficient lignin bioconversion process, where solubilized lignin from laccase–HBT treatment served as a superior substrate for bioconversion by Rhodococcus opacus PD630. The cell growth was increased by 10⁶ fold, and the lipid titer reached 1.02 g/L. Overall, the study has manifested that an efficient enzyme–mediator–microbial system can be exploited to establish a bioprocess to solubilize lignin, cleave lignin linkages, modify the structure, and produce substrates amenable to bioconversion.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE), Office of Sustainable Transportation. Bioenergy Technologies Office (BETO)

Grant/Contract Number:: AC05-00OR22725; EE0006112

OSTI ID:: 1344299

Alternate ID(s):: OSTI ID: 2532427

Journal Information:: ACS Sustainable Chemistry & Engineering, Journal Name: ACS Sustainable Chemistry & Engineering Journal Issue: 3 Vol. 5; ISSN 2168-0485

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (40)

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
Biodegradation of kraft lignin by a newly isolated bacterial strain, Aneurinibacillus aneurinilyticus from the sludge of a pulp paper mill Raj, Abhay; Chandra, Ram; Reddy, M. M. K. World Journal of Microbiology and Biotechnology, Vol. 23, Issue 6 https://doi.org/10.1007/s11274-006-9299-x	journal	November 2006
Oxidation of non-phenolic substrates: An expanded role for laccase in lignin biodegradation Bourbonnais, Robert; Paice, Michael G. FEBS Letters, Vol. 267, Issue 1 https://doi.org/10.1016/0014-5793(90)80298-W	journal	July 1990
A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase Eggert, Claudia; Temp, Ulrike; Dean, Jeffrey F. D. FEBS Letters, Vol. 391, Issue 1-2 https://doi.org/10.1016/0014-5793(96)00719-3	journal	August 1996
Aromatic ring cleavage of a non-phenolic β- O -4 lignin model dimer by laccase of Trametes versicolor in the presence of 1-hydroxybenzotriazole Kawai, Shingo; Nakagawa, Makoto; Ohashi, Hideo FEBS Letters, Vol. 446, Issue 2-3 https://doi.org/10.1016/S0014-5793(99)00247-1	journal	March 1999
Residual lignin studies of laccase-delignified kraft pulps Sealey, J.; Ragauskas, A. J. Enzyme and Microbial Technology, Vol. 23, Issue 7-8 https://doi.org/10.1016/S0141-0229(98)00056-8	journal	November 1998
Degradation of nonphenolic lignin by the laccase/1-hydroxybenzotriazole system Srebotnik, Ewald; Hammel, Kenneth E. Journal of Biotechnology, Vol. 81, Issue 2-3 https://doi.org/10.1016/S0168-1656(00)00303-5	journal	August 2000
Electrochemical analysis of the interactions of laccase mediators with lignin model compounds Bourbonnais, Robert; Leech, Dónal; Paice, Michael G. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1379, Issue 3 https://doi.org/10.1016/S0304-4165(97)00117-7	journal	March 1998
Efficient coagulation of microalgae in cultures with filamentous fungi Xie, Shangxian; Sun, Su; Dai, Susie Y. Algal Research, Vol. 2, Issue 1 https://doi.org/10.1016/j.algal.2012.11.004	journal	January 2013
Towards industrially-feasible delignification and pitch removal by treating paper pulp with Myceliophthora thermophila laccase and a phenolic mediator Babot, Esteban D.; Rico, Alejandro; Rencoret, Jorge Bioresource Technology, Vol. 102, Issue 12 https://doi.org/10.1016/j.biortech.2011.03.100	journal	June 2011
Industrial and biotechnological applications of laccases: A review Rodríguez Couto, Susana; Toca Herrera, José Luis Biotechnology Advances, Vol. 24, Issue 5 https://doi.org/10.1016/j.biotechadv.2006.04.003	journal	September 2006
Exploration of Natural Biomass Utilization Systems (NBUS) for advanced biofuel—from systems biology to synthetic design Xie, Shangxian; Syrenne, Ryan; Sun, Su Current Opinion in Biotechnology, Vol. 27 https://doi.org/10.1016/j.copbio.2014.02.007	journal	June 2014
Comparison of a series of laccase mediators in the electro-oxidation reactions of non-phenolic lignin model compounds Shiraishi, Takumi; Sannami, Yumi; Kamitakahara, Hiroshi Electrochimica Acta, Vol. 106 https://doi.org/10.1016/j.electacta.2013.05.112	journal	September 2013
High-cell-density batch fermentation of Rhodococcus opacus PD630 using a high glucose concentration for triacylglycerol production Kurosawa, Kazuhiko; Boccazzi, Paolo; de Almeida, Naomi M. Journal of Biotechnology, Vol. 147, Issue 3-4 https://doi.org/10.1016/j.jbiotec.2010.04.003	journal	June 2010
Enhanced transformation of triclosan by laccase in the presence of redox mediators Murugesan, Kumarasamy; Chang, Yoon-Young; Kim, Young-Mo Water Research, Vol. 44, Issue 1 https://doi.org/10.1016/j.watres.2009.09.058	journal	January 2010
Strategies for the Conversion of Lignin to High-Value Polymeric Materials: Review and Perspective Upton, Brianna M.; Kasko, Andrea M. Chemical Reviews, Vol. 116, Issue 4, p. 2275-2306 https://doi.org/10.1021/acs.chemrev.5b00345	journal	December 2015
Understanding Pulp Delignification by Laccase–Mediator Systems through Isolation and Characterization of Lignin–Carbohydrate Complexes Du, Xueyu; Li, Jiebing; Gellerstedt, Göran Biomacromolecules, Vol. 14, Issue 9 https://doi.org/10.1021/bm4006936	journal	August 2013
Investigation of the Molecular Weight Increase of Commercial Lignosulfonates by Laccase Catalysis Areskogh, Dimitri; Li, Jiebing; Gellerstedt, Göran Biomacromolecules, Vol. 11, Issue 4 https://doi.org/10.1021/bm901258v	journal	April 2010
Oxidative Mechanisms Involved in Lignin Degradation by White-Rot Fungi ten Have, Rimko; Teunissen, Pauline J. M. Chemical Reviews, Vol. 101, Issue 11 https://doi.org/10.1021/cr000115l	journal	November 2001
Analysis of total phenols using the Prussian Blue method Budini, Rolando; Tonelli, Domenica; Girotti, Stefano Journal of Agricultural and Food Chemistry, Vol. 28, Issue 6 https://doi.org/10.1021/jf60232a056	journal	November 1980
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
Adipic acid production from lignin Vardon, Derek R.; Franden, Mary Ann; Johnson, Christopher W. Energy & Environmental Science, Vol. 8, Issue 2 https://doi.org/10.1039/C4EE03230F	journal	January 2015
Simultaneous conversion of all cell wall components by an oleaginous fungus without chemi-physical pretreatment Xie, Shangxian; Qin, Xing; Cheng, Yanbing Green Chemistry, Vol. 17, Issue 3 https://doi.org/10.1039/C4GC01529K	journal	January 2015
Bioconversion of oxygen-pretreated Kraft lignin to microbial lipid with oleaginous Rhodococcus opacus DSM 1069 Wei, Zhen; Zeng, Guangming; Huang, Fang Green Chemistry, Vol. 17, Issue 5 https://doi.org/10.1039/C5GC00422E	journal	January 2015
Synergistic enzymatic and microbial lignin conversion Zhao, Cheng; Xie, Shangxian; Pu, Yunqiao Green Chemistry, Vol. 18, Issue 5 https://doi.org/10.1039/C5GC01955A	journal	January 2016
New insights into the structure and composition of technical lignins: a comparative characterisation study Constant, Sandra; Wienk, Hans L. J.; Frissen, Augustinus E. Green Chemistry, Vol. 18, Issue 9 https://doi.org/10.1039/C5GC03043A	journal	January 2016
Application of quantitative 31P NMR in biomass lignin and biofuel precursors characterization Pu, Yunqiao; Cao, Shilin; Ragauskas, Arthur J. Energy & Environmental Science, Vol. 4, Issue 9 https://doi.org/10.1039/c1ee01201k	journal	January 2011
Enzymatic cleavage of lignin β-O-4 aryl ether bonds via net internal hydrogen transfer Reiter, Jochen; Strittmatter, Harald; Wiemann, Lars O. Green Chemistry, Vol. 15, Issue 5 https://doi.org/10.1039/c3gc40295a	journal	January 2013
Lignin to lipid bioconversion by oleaginous Rhodococci Kosa, Matyas; Ragauskas, Arthur J. Green Chemistry, Vol. 15, Issue 8 https://doi.org/10.1039/c3gc40434j	journal	January 2013
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
Lignin Conversion: Opportunities and Challenges for the Integrated Biorefinery Xie, Shangxian; Ragauskas, Arthur J.; Yuan, Joshua S. Industrial Biotechnology, Vol. 12, Issue 3 https://doi.org/10.1089/ind.2016.0007	journal	June 2016
Degradation of a non-phenolic Î²- O -4 substructure and of polymeric lignin model compounds by laccase of Coriolus versicolor in the presence of 1-hydroxybenzotriazole Kawai, Shingo; Asukai, Masanori; Ohya, Noriko FEMS Microbiology Letters, Vol. 170, Issue 1 https://doi.org/10.1111/j.1574-6968.1999.tb13354.x	journal	January 1999
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
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
Comparison of Fungal Laccases and Redox Mediators in Oxidation of a Nonphenolic Lignin Model Compound Li, Kaichang; Xu, Feng; Eriksson, Karl-Erik L. Applied and Environmental Microbiology, Vol. 65, Issue 6 https://doi.org/10.1128/AEM.65.6.2654-2660.1999	journal	June 1999
Recent Development in Chemical Depolymerization of Lignin: A Review Wang, Hai; Tucker, Melvin; Ji, Yun Journal of Applied Chemistry, Vol. 2013, p. 1-9 https://doi.org/10.1155/2013/838645	journal	January 2013
Lignin monomer composition affects Arabidopsis cell-wall degradability after liquid hot water pretreatment Li, Xu; Ximenes, Eduardo; Kim, Youngmi Biotechnology for Biofuels, Vol. 3, Issue 1 https://doi.org/10.1186/1754-6834-3-27	journal	January 2010
The fate of lignin during hydrothermal pretreatment Trajano, Heather L.; Engle, Nancy L.; Foston, Marcus Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-110	journal	January 2013
Pretreatment with laccase and a phenolic mediator degrades lignin and enhances saccharification of Eucalyptus feedstock Rico, Alejandro; Rencoret, Jorge; del Río, José C. Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-6	journal	January 2014
Recent Advances in Characterization of Lignin Polymer by Solution-State Nuclear Magnetic Resonance (NMR) Methodology Wen, Jia-Long; Sun, Shao-Long; Xue, Bai-Liang Materials, Vol. 6, Issue 1 https://doi.org/10.3390/ma6010359	journal	January 2013

Cited By (15)

Catalytic Performance of Food Additives Alum, Flocculating Agent, Al(SO₄)₃, AlCl₃, and Other Lewis Acids in Microwave Solvolysis of Hardwoods and Recalcitrant Softwood for Biorefinery Ohashi, Yasunori; Watanabe, Takashi ACS Omega, Vol. 3, Issue 11 https://doi.org/10.1021/acsomega.8b01454	journal	November 2018
A highly stable laccase obtained by swapping the second cupredoxin domain Pardo, Isabel; Rodríguez-Escribano, David; Aza, Pablo Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-34008-3	journal	October 2018
A bionic system with Fenton reaction and bacteria as a model for bioprocessing lignocellulosic biomass Zhang, Kejing; Si, Mengying; Liu, Dan Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1035-x	journal	February 2018
Discovery of potential pathways for biological conversion of poplar wood into lipids by co-fermentation of Rhodococci strains Li, Xiaolu; He, Yucai; Zhang, Libing Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1395-x	journal	March 2019
Mechanism‐Guided Design of Highly Efficient Protein Secretion and Lipid Conversion for Biomanufacturing and Biorefining Xie, Shangxian; Sun, Su; Lin, Furong Advanced Science https://doi.org/10.1002/advs.201801980	journal	May 2019
The current and emerging sources of technical lignins and their applications: Sources of Technical Lignins Li, Tao; Takkellapati, Sudhakar Biofuels, Bioproducts and Biorefining, Vol. 12, Issue 5 https://doi.org/10.1002/bbb.1913	journal	July 2018
Biotransformation of lignin: Mechanisms, applications and future work Li, Xiang; Zheng, Yi Biotechnology Progress, Vol. 36, Issue 1 https://doi.org/10.1002/btpr.2922	journal	October 2019
Non‐Solvent Fractionation of Lignin Enhances Carbon Fiber Performance Li, Qiang; Li, Mengjie; Lin, Hao‐Sheng ChemSusChem, Vol. 12, Issue 14 https://doi.org/10.1002/cssc.201901052	journal	June 2019
Effect of Novel Pretreatment of Steam Explosion Associated with Ammonium Sulfite Process on Enzymatic Hydrolysis of Corn Straw Zhao, Qihong; Wang, Lan; Chen, Hongzhang Applied Biochemistry and Biotechnology, Vol. 189, Issue 2 https://doi.org/10.1007/s12010-019-03018-w	journal	May 2019
Chemicals from lignin: an interplay of lignocellulose fractionation, depolymerisation, and upgrading Schutyser, W.; Renders, T.; Van den Bosch, S. Chemical Society Reviews, Vol. 47, Issue 3 https://doi.org/10.1039/c7cs00566k	journal	January 2018
Cooperative valorization of lignin and residual sugar to polyhydroxyalkanoate (PHA) for enhanced yield and carbon utilization in biorefineries Liu, Zhi-Hua; Shinde, Somnath; Xie, Shangxian Sustainable Energy & Fuels, Vol. 3, Issue 8 https://doi.org/10.1039/c9se00021f	journal	January 2019
Structural Characterization of Lignin and Its Degradation Products with Spectroscopic Methods Lu, Yao; Lu, Yong-Chao; Hu, Hong-Qin Journal of Spectroscopy, Vol. 2017 https://doi.org/10.1155/2017/8951658	journal	January 2017
Lipid metabolism of phenol-tolerant Rhodococcus opacus strains for lignin bioconversion Henson, William R.; Hsu, Fong-Fu; Dantas, Gautam Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1337-z	journal	December 2018
Development of Rhodococcus opacus as a chassis for lignin valorization and bioproduction of high-value compounds Anthony, Winston E.; Carr, Rhiannon R.; DeLorenzo, Drew M. Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1535-3	journal	August 2019
Alternatives for Chemical and Biochemical Lignin Valorization: Hot Topics from a Bibliometric Analysis of the Research Published During the 2000–2016 Period Abejón, Ricardo; Pérez-Acebo, Heriberto; Clavijo, Leonardo Processes, Vol. 6, Issue 8 https://doi.org/10.3390/pr6080098	journal	July 2018

Similar Records

A Review on The Bioconversion of Lignin to Microbial Lipid with Oleaginous Rhodococcus opacus

Journal Article · Thu Jun 29 00:00:00 EDT 2017 · Journal of Biotechnology & Biomaterials · OSTI ID:1376594

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
59 BASIC BIOLOGICAL SCIENCES
Rhodococcus
bioconversion
laccase−mediator−microbial
lignin
valorization

Advanced Chemical Design for Efficient Lignin Bioconversion

Citation Formats

References (40)

Cited By (15)

Similar Records

Related Subjects