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Efficient, environmentally-friendly and specific valorization of lignin: promising role of non-radical lignolytic enzymes

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Abstract

Lignin is the second most abundant bio-resource in nature. It is increasingly important to convert lignin into high value-added chemicals to accelerate the development of the lignocellulose biorefinery. Over the past several decades, physical and chemical methods have been widely explored to degrade lignin and convert it into valuable chemicals. Unfortunately, these developments have lagged because of several difficulties, of which high energy consumption and non-specific cleavage of chemical bonds in lignin remain the greatest challenges. A large number of enzymes have been discovered for lignin degradation and these are classified as radical lignolytic enzymes and non-radical lignolytic enzymes. Radical lignolytic enzymes, including laccases, lignin peroxidases, manganese peroxidases and versatile peroxidases, are radical-based bio-catalysts, which degrade lignins through non-specific cleavage of chemical bonds but can also catalyze the radical-based re-polymerization of lignin fragments. In contrast, non-radical lignolytic enzymes selectively cleave chemical bonds in lignin and lignin model compounds and, thus, show promise for use in the preparation of high value-added chemicals. In this mini-review, recent developments on non-radical lignolytic enzymes are discussed. These include recently discovered non-radical lignolytic enzymes, their metabolic pathways for lignin conversion, their recent application in the lignin biorefinery, and the combination of bio-catalysts with physical/chemical methods for industrial development of the lignin refinery.

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References

  • Abe T, Masai E, Miyauchi K, Katayama Y, Fukuda M (2005) A tetrahydrofolate-dependent O-demethylase, LigM, is crucial for catabolism of vanillate and syringate in Sphingomonas paucimobilis SYK-6. J Bacteriol 187:2030–2037

    Article  CAS  Google Scholar 

  • Asano Y, Yamamoto Y, Yamada H (1994) Catechol 2,3-dioxygenase-catalyzed synthesis of picolinic acids from catechols. Biosci Biotechnol Biochem 58:2054–2056

    Article  Google Scholar 

  • Bains J, Boulanger MJ (2007) Biochemical and structural characterization of the paralogous benzoate CoA ligases from Burkholderia xenovorans LB400: Defining the entry point into the novel benzoate oxidation (box) pathway. J Mol Biol 373:965–977

    Article  CAS  Google Scholar 

  • Barghini P, Di Gioia D, Fava F, Ruzzi M (2007) Vanillin production using metabolically engineered Escherichia coli under non-growing conditions. Microb Cell Factories 6:13. doi:10.1186/1475-2859-6-13

    Article  Google Scholar 

  • Bugg TD, Ahmad M, Hardiman EM, Rahmanpour R (2011a) Pathways for degradation of lignin in bacteria and fungi. Nat Product Rep 28:1883–1896

    Article  CAS  Google Scholar 

  • Bugg TD, Ahmad M, Hardiman EM, Singh R (2011b) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22:394–400

    Article  CAS  Google Scholar 

  • Chi Y, Hatakka A, Maijala P (2007) Can co-culturing of two white-rot fungi increase lignin degradation and the production of lignin-degrading enzymes? Int Biodeterior Biodegrad 59(1):32–39

    Article  CAS  Google Scholar 

  • Davis KM, Rover M, Brown RC, Bai XL, Wen ZY, Jarboe LR (2016) Recovery and utilization of lignin monomers as part of the biorefinery approach. Energies 9:808. doi:10.3390/en9100808

    Article  Google Scholar 

  • Falconnier B, Lapierre C, Lesage-Meessen L, Yonnet G, Brunerie P, Ceccaldi BC, Corrieu G, Asther M (1994) Vanillin as a product of ferulic acid biotransformation by the white rot fungus Pycnoporus cinnabarinus I-37: identification of metabolic pathways. J Biotechnol 37:123–132

    Article  CAS  Google Scholar 

  • Fuchs G, Boll M, Heider J (2011) Microbial degradation of aromatic compounds—from one strategy to four. Nat Rev Microbiol 9:803–816. doi:10.1038/nrmicro2652

    Article  CAS  Google Scholar 

  • Gall DL, Ralph J, Donohue TJ, Noguera DR (2014) A group of sequence-related sphingomonad enzymes catalyzes cleavage of β-aryl ether linkages in lignin β-guaiacyl and β-syringyl ether dimers. Environ Sci Technol 48(20):12454–12463

    Article  CAS  Google Scholar 

  • Gallage NJ, Hansen EH, Kannangara R, Olsen CE, Motawia MS, Jørgensen K, Holme I, Hebelstrup K, Grisoni M, Møller BL (2014) Vanillin formation from ferulic acid in Vanilla planifolia is catalyzed by a single enzyme. Nat Commun 5:4037

    Article  CAS  Google Scholar 

  • Gosling A, Fowler SJ, O’Shea MS, Straffon M, Dumsday G, Zachariou M (2011) Metabolic production of a novel polymer feedstock, 3-carboxy muconate, from vanillin. Appl Microbiol Biotechnol 90:107–116

    Article  CAS  Google Scholar 

  • Gupta JK, Hamp SG, Buswell JA, Eriksson KE (1981) Metabolism of trans-ferulic acid by white-rot fungus Sporotrichum pulverulentum. Arch Microbiol 128:349–354

    Article  Google Scholar 

  • Han L, Liu P, Sun J, Wu Y, Zhang Y, Chen W, Lin J, Wang Q, Ma Y (2015) Engineering catechol 1,2-dioxygenase by design for improving the performance of the cis, cis-muconic acid synthetic pathway in Escherichia coli. Sci Rep 5:13435. doi:10.1038/srep13435

    Article  CAS  Google Scholar 

  • Harwood CS, Parales RE (1996) The β-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50(1):553–590. doi:10.1146/annurev.micro.50.1.553

    Article  CAS  Google Scholar 

  • Helmich KE, Pereira JH, Gall DL, Heins RA, McAndrew RP, Bingman C, Deng K, Holland KC, Noguera DR, Simmons BA, Sale KennethL, Ralph J, Donohue TJ, Adams PD, Phillips GN Jr (2016) Structural basis of stereospecificity in the bacterial enzymatic cleavage of β-aryl ether bonds in lignin. J Biol Chem 291:5234–5246. doi:10.1074/jbc.M115.694307

    Article  CAS  Google Scholar 

  • Huang DL, Zeng GM, Feng CL, Hu S, Lai C, Zhao MH, Su FF, Tang L, Liu HL (2010) Changes of microbial population structure related to lignin degradation during lignocellulosic waste composting. Bioresour Technol 101(11):4062–4067

    Article  CAS  Google Scholar 

  • Huo Y, Zeng H, Zhang Y (2016) Integrating metabolic engineering and heterogeneous chemocatalysis: New opportunities for biomass to chemicals. ChemSusChem 9:1078–1080

    Article  CAS  Google Scholar 

  • Iwabuchi N, Takiguchi H, Hamaguchi T, Takihara H, Sunairi M, Matsufuji H (2015) Transformation of lignin-derived aromatics into nonaromatic polymeric substances with fluorescent activities (NAPSFA) by Pseudomonas sp. ITH-SA-1. ACS Sustain Chem Eng 3:2678–2685

    Article  CAS  Google Scholar 

  • Jiménez JI, Miñambres B, García JL, Díaz E (2002) Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 4:824–841

    Article  Google Scholar 

  • Johnson CW, Beckham GT (2015) Aromatic catabolic pathway selection for optimal production of pyruvate and lactate from lignin. Metab Eng 28:240–247. doi:10.1016/j.ymben.2015.01.005

    Article  CAS  Google Scholar 

  • Johnson CW, Salvachúa D, Khanna P, Smith H, Peterson DJ, Beckham GT (2016) Enhancing muconic acid production from glucose and lignin-derived aromatic compounds via increased protocatechuate decarboxylase activity. Metab Eng Commun 3:111–119

    Article  Google Scholar 

  • Jung DH, Kim EJ, Jung E, Kazlauskas RJ, Choi KY, Kim BG (2016) Production of p-hydroxybenzoic acid from p-coumaric acid by Burkholderia glumae BGR1. Biotechnol Bioeng 113(7):1493–1503

    Article  CAS  Google Scholar 

  • Jurkovfid M, Wurst M (1993) Biodegradation of aromatic carboxylic acids by Pseudomonas mira. FEMS Microbiol Lett 111:245–250

    Article  Google Scholar 

  • Kadakol C, Kamanavalli CM (2010) Biodegradation of eugenol by Bacillus cereus strain PN24. J Chem 7:474–480

    Google Scholar 

  • Karmakar B, Vohra RM, Nandanwar H, Sharma P, Gupta KG, Sobti RC (2000) Rapid degradation of ferulic acid via 4-vinylguaiacol and vanillin by a newly isolated strain of Bacillus coagulans. J Biotechnol 80:195–202

    Article  CAS  Google Scholar 

  • Kasai D, Masai E, Miyauchi K, Katayama Y, Fukuda M (2004) Characterization of the 3-O-methylgallate dioxygenase gene and evidence of multiple 3-O-methylgallate catabolic pathways in Sphingomonas paucimobilis SYK-6. J Bacteriol 186:4951–4959

    Article  CAS  Google Scholar 

  • Kasai D, Kamimura N, Tani K, Umeda S, Abe T, Fukuda M, Masai E (2012) Characterization of FerC, a MarR-type transcriptional regulator, involved in transcriptional regulation of the ferulate catabolic operon in Sphingobium sp. strain SYK-6. FEMS Microbiol Lett 332:68–75

    Article  CAS  Google Scholar 

  • Kaur B, Chakraborty D (2013) Biotechnological and molecular approaches for vanillin production: a review. Appl Biochem Biotechnol 169:1353–1372

    Article  CAS  Google Scholar 

  • Kosa M, Ragauskas AJ (2012) Bioconversion of lignin model compounds with oleaginous Rhodococci. Appl Microbiol Biotechnol 93:891–900

    Article  CAS  Google Scholar 

  • Kosa M, Ragauskas AJ (2013) Lignin to lipid bioconversion by oleaginous Rhodococci. Green Chem 15:2070–2074

    Article  CAS  Google Scholar 

  • Labuda IM, Goers SK, Keon KA (1992) Bioconversion process for the production of vanillin. Patent application US 5128253

  • Lee EG, Yoon SH, Das A, Lee SH, Li C, Kim JY, Choi MS, Oh DK, Kim SW (2009) Directing vanillin production from ferulic acid by increased acetyl-CoA consumption in recombinant Escherichia coli. Biotechnol Bioeng 102:200–208

    Article  CAS  Google Scholar 

  • Linger JG, Vardon, DR, Guarnieri MT, Karp EM, Hunsinger GB, Franden MA, Johnson CW, Chupka G, Strathmann TJ, Pienkos PT, Beckham GT (2014). Lignin valorization through integrated biological funneling and chemical catalysis. PNAS 111:12013–12018.doi:10.1073/pnas.1410657111

    Article  CAS  Google Scholar 

  • Lupa B, Lyon D, Shaw LN, Sieprawska-Lupa M, Wiegel J (2008) Properties of the reversible nonoxidative vanillate/4-hydroxybenzoate decarboxylase from Bacillus subtilis. Can J Microbiol 54:75–81

    Article  CAS  Google Scholar 

  • Masai E, Kubota S, Katayama Y, Kawai S, Yamasaki M, Morohoshi N (1993) Characterization of the Cα-dehydrogenase gene involved in the cleavage of β-aryl ether by Pseudomonas paucimohilis. Biosci Biotechnol Biochem 57:1655–1659

    Article  CAS  Google Scholar 

  • Masai E, Yamamoto Y, Inoue T, Takamura K, Hara H, Kasai D, Katayama Y, Fukuda M (2007a) Characterization of ligV essential for catabolism of vanillin by Sphingomonas paucimobilis SYK-6. Biosci Biotechnol Biochem 71:2487–2892. doi:10.1271/bbb.70267

    Article  CAS  Google Scholar 

  • Masai E, Katayama Y, Fukuda M (2007b) Genetic and biochemical investigations on bacterial catabolic pathwaysfor lignin-derived aromatic compounds. Biosci Biotechnol Biochem 71:1–15

    Article  CAS  Google Scholar 

  • Meijnen JP, Verhoef S, Briedjlal AA, de Winde JH, Ruijssenaars HJ (2011) Improved p-hydroxybenzoic acid production by engineered Pseudomonas putida S12 by using a mixed-substrate feeding strategy. Appl Microbiol Biotechnol 90:885–893

    Article  CAS  Google Scholar 

  • Meux E, Prosper P, Masai E, Mulliert G, Dumarcay S, Morel M, Didierjean C, Gelhaye E, Favier F (2012) Sphingobium sp. SYK-6 LigG involved in lignin degradation is structurally and biochemically related to the glutathione transferase omega class. FEBS Lett 586:3944–3950. doi:10.1016/j.febslet.2012.09.036

    Article  CAS  Google Scholar 

  • Mukherjee G, Sachan A, Ghosh S, Mitra A (2006) Conversion of sinapic acid to syringic acid by a filamentous fungus Paecilomyces variotii. J Gen Appl Microbiol 52:131–135

    Article  CAS  Google Scholar 

  • Mycroft Z, Gomis M, Mines P, Law P, Bugg TD (2015) Biocatalytic conversion of lignin to aromatic dicarboxylic acids in Rhodococcus jostii RHA1 by re-routing aromatic degradation pathways. Green Chem 17:4974–4979

    Article  CAS  Google Scholar 

  • Nazareth S, Mavinkurve S (1986) Degradation of ferulic acid via 4-vinylguaiacol by Fusarium solani (Mart) Sacc. Can J Microbiol 32:494–497

    Article  CAS  Google Scholar 

  • Ohta Y, Nishi S, Hasegawa R, Hatada Y (2015) Combination of six enzymes of a marine Novosphingobium converts the stereoisomers of beta-O-4 lignin model dimers into the respective monomers. Sci Rep 5:15105. doi:10.1038/srep15105

    Article  CAS  Google Scholar 

  • Okamura-Abe Y, Abe T, Nishimura K, Kawata Y, Sato-Izawa K, Otsuka Y, Nakamura M, Kajita S, Masai E, Sonoki T, Katayama Y (2016) Beta-ketoadipic acid and muconolactone production from a lignin-related aromatic compound through the protocatechuate 3,4-metabolic pathway. J Biosci Bioeng 121:652–658

    Article  CAS  Google Scholar 

  • Otsuka Y, Nakamura M, Shigehara K, Sugimura K, Masai E, Ohara S, Katayama Y (2006) Efficient production of 2-pyrone 4,6-dicarboxylic acid as a novel polymer-based material from protocatechuate by microbial function. Appl Microbiol Biotechnol 71:608–614

    Article  CAS  Google Scholar 

  • Pan C, Oda Y, Lankford PK, Zhang B, Samatova FN, Pelletier AD, Harwood SC, Hettich LR (2008) Characterization of anaerobic catabolism of p-coumarate in Rhodopseudomonas palustris by integrating transcriptomics and quantitative proteomics. Mol Cell Proteom 7:938–948

    Article  CAS  Google Scholar 

  • Peng X, Misawa N, Harayama S (2003) Isolation and characterization of Thermophilic Bacilli degrading cinnamic, 4-coumaric, and ferulic acids. Appl Environ Microbiol 69:1417–1427

    Article  CAS  Google Scholar 

  • Pereira JH, Heins RA, Gall DL, Mcandrew RP, Deng K, Holland KC, Donohue TJ, Noguera DR, Simmons BA, Sale KL, Ralph J, Adams PD (2016) Structural and biochemical characterization of the early and late enzymes in the lignin β-aryl ether cleavage pathway from Sphingobium sp. SYK-6. J Biol Chem 291:10228–10238. doi:10.1074/jbc.M115.700427

    Article  CAS  Google Scholar 

  • Pérez -Pantoja D, Donoso R, Agulló L, Córdova M, Seeger M, Pieper DH, González B (2012) Genomic analysis of the potential for aromatic compounds biodegradation in Burkholderiales. Environ Microbiol 14:1091–1117

    Article  Google Scholar 

  • Picart P, Mueller C, Mottweiler J, Wiermans L, Bolm C, Dominguez de Maria P, Schallmey A (2014) From gene towards selective biomass valorization: bacterial beta-etherases with catalytic activity on lignin-like polymers. Chemsuschem 7:3164–3171

    Article  CAS  Google Scholar 

  • Picart P, Dominguez de Maria P, Schallmey A (2015) From gene to biorefinery: microbial β-etherases as promising biocatalysts for lignin valorization. Front Microbiol 6:916. doi:10.3389/fmicb.2015.00916

    Article  Google Scholar 

  • Plaggenborg R, Overhage J, Loos A, Archer JAC, Lessard P, Sinskey AJ, Steinbuchel A, Priefert H (2006) Potential of Rhodococcus strains for biotechnological vanillin production from ferulic acid and eugenol. Appl Microbiol Biotechnol 72:745–755

    Article  CAS  Google Scholar 

  • Pollegioni L, Tonin F, Rosini E (2015) Lignin-degrading enzymes. FEBS J 282:1190–1213. doi:10.1111/febs.13224

    Article  CAS  Google Scholar 

  • Priefert H, Rabenhorst J, Steinbüchel A (2001) Biotechnological production of vanillin. Appl Microbiol Biotechnol 56:296–314

    Article  CAS  Google Scholar 

  • Rahimi A, Ulbrich A, Coon JJ, Stahl SS (2014) Formic-acid-induced depolymerization of oxidized lignin to aromatics. Nature 515:249–252. doi:10.1038/nature13867

    Article  CAS  Google Scholar 

  • Reiter J, Strittmatter H, Wiemann LO, Schieder D, Sieber V (2013) Enzymatic cleavage of lignin β-O-4 aryl ether bonds via net internal hydrogen transfer. Green Chem 15:1373–1381

    Article  CAS  Google Scholar 

  • Rosazza JP, Huang Z, Dostal L, Volm T, Rousseau B (1995) Biocatalytic transformations of ferulic acid: an abundant aromatic natural product. J Ind Microbiol 15:457–471

    Article  CAS  Google Scholar 

  • Sainsbury PD, Hardiman EM, Ahmad M, Otani H, Seghezzi N, Eltis LD, Bugg TDH (2013) Breaking down lignin to high-value chemicals: the conversion of lignocellulose to vanillin in a gene deletion mutant of Rhodococcus jostii RHA1. ACS Chem Biol 8:2151–2156

    Article  CAS  Google Scholar 

  • Sato Y, Moriuchi H, Hishiyama S, Otsuka Y, Oshima K, Kasai D, Nakamura M, Ohara S, Katayama Y, Fukuda M, Masai E (2009) Identification of three alcohol dehydrogenase genes involved in the stereospecific catabolism of arylglycerol-β-aryl ether by sphingobium sp. strain SYK-6. Appl Environ Microbiol 75(16):5195–5201

    Article  CAS  Google Scholar 

  • Schwartz TJ, O’Neill BJ, Shanks BH, Dumesic JA (2014) Bridging the chemical and biological catalysis gap: challenges and outlooks for producing sustainable chemicals. ACS Catal 4:2060–2069

    Article  CAS  Google Scholar 

  • Shuai L, Amiri MT, Questell-Santiago YM, Héroguel F, Li Y, Kim H, Meilan R, Chapple C, Ralph J, Luterbacher JS (2016) Formaldehyde stabilization facilitates lignin monomer production during biomass depolymerization. Science 354:329–333. doi:10.1126/science.aaf7810

    Article  CAS  Google Scholar 

  • Sonoki T, Morooka M, Sakamoto K, Otsuka Y, Nakamura M, Jellison J, Goodell B (2014) Enhancement of protocatechuate decarboxylase activity for the effective production of muconate from lignin-related aromatic compounds. J Biotechnol 192:71–77

    Article  CAS  Google Scholar 

  • Tilay A, Bule M, Annapure U (2010) Production of biovanillin by one-step biotransformation using fungus Pycnoporous cinnabarinus. J Agric Food Chem 58:4401–4405

    Article  CAS  Google Scholar 

  • Trautwein K, Wilkes H, Rabus R (2012) Proteogenomic evidence for β-oxidation of plant-derived 3-phenylpropanoids in “Aromatoleum aromaticum” EbN1. Proteomics 12:1402–1413

    Article  CAS  Google Scholar 

  • van Duuren JB, Wijte D, Karge B, dos Santos VA, Yang Y, Mars AE, Eggink G (2012) pH-stat fed-batch process to enhance the production of cis,cis-muconate from benzoate by Pseudomonas putida KT2440-JD1. Biotechnol Prog 28:85–92

    Article  Google Scholar 

  • Vardon DR, Franden MA, Johnson CW, Karp EM, Guarnieri MT, Linger JG, Salm MJ, Strathmann TJ, Beckham GT (2015) Adipic acid production from lignin. Energy Environ Sci 8:617–628. doi:10.1039/c4ee03230f

    Article  CAS  Google Scholar 

  • Vardon DR, Rorrer NA, Salvachúa D, Settle AE, Johnson CW, Menart MJ, Cleveland NS, Ciesielski PN, Steirer KX, Dorgan JR, Beckham GT (2016) cis, cis-Muconic acid: separation and catalysis to bio-adipic acid for nylon-6, 6 polymerization. Green Chem 18:3397–3413

    Article  CAS  Google Scholar 

  • Wang C, Ouyang XH, Su SS, Liang X, Zhang C, Wang WY, Yuan QP, Li Q (2016) Effect of sulfonated lignin on enzymatic activity of the lignolytic enzymes C α -dehydrogenase LigD and β-etherase LigF. Enzyme Microb Technol 93:59–69

    Article  Google Scholar 

  • Wong DWS (2009) Structure and action mechanism of ligninolytic enzymes. Appl Biochem Biotech 157:174–209. doi:10.1007/s12010-008-8279-z

    Article  CAS  Google Scholar 

  • Xie T, Liu ZC, Liu Q, Wang GG (2015) Structural insight into the oxidation of sinapic acid by CotA laccase. J Struc Biol 190:155–161. doi:10.1016/j.jsb.2015.03.005

    Article  CAS  Google Scholar 

  • Xie XG, Huang CY, Fu WQ, Dai CC (2016) Potential of endophytic fungus Phomopsis liquidambari for transformation and degradation of recalcitrant pollutant sinapic acid. Fungal Biol 120:402–413

    Article  CAS  Google Scholar 

  • Yamada M, Okada Y, Yoshida T, Nagasawa T (2007) Biotransformation of isoeugenol to vanillin by Pseudomonas putida IE27 cells. Appl Microbiol Biotechnol 73:1025–1030

    Article  CAS  Google Scholar 

  • Zhao C, Xie S, Pu Y, Zhang R, Huang F, Ragauskas AJ, Yuan JS (2015) Synergistic enzymatic and microbial lignin conversion. Green Chem 18:1306–1312

    Article  Google Scholar 

Download references

Acknowledgements

We thank the National Key Research Programme (2016YFD0400601), State Key Laboratory of Pulp and Paper Engineering (201760), Natural Science Foundation of China (NSFC 21576153), Beijing Natural Science Foundation (5162019), National High-tech Research and Development Program (2015AA021001) and Chinese 111 Project (B13005) for the generous financial support.

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Correspondence to Wenya Wang.

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Wenya Wang and Chao Zhang have contributed equally to this work.

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Wang, W., Zhang, C., Sun, X. et al. Efficient, environmentally-friendly and specific valorization of lignin: promising role of non-radical lignolytic enzymes. World J Microbiol Biotechnol 33, 125 (2017). https://doi.org/10.1007/s11274-017-2286-6

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