Understanding lignin biodegradation for the improved utilization of plant biomass in mod ern biorefineries

Biofuels, Bioproducts and Biorefining

Volumn 8, Issue 5, 2014, Pages 615-625

  Camarero, Susana ^a   Martínez, María Jesús ^a   Martínez, Angel T ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

Author keywords

Biorefinery; Lignin biodegradation; Ligninolytic peroxidases; Plant biomass; White biotechnology; White rot fungi; laccases

Indexed keywords

BIOMASS; BIOTECHNOLOGY; ENVIRONMENTAL IMPACT; ENZYMES; FUNGI; INDUSTRIAL CHEMICALS; LIGNIN; LIGNOCELLULOSIC BIOMASS; MOLECULAR BIOLOGY; PAPER AND PULP INDUSTRY; PAPER AND PULP MILLS; REFINING; WOOD;

BIOREFINERIES; LACCASES; LIGNIN BIODEGRADATION; LIGNINOLYTIC PEROXIDASES; PLANT BIOMASS; WHITE BIOTECHNOLOGY;

BIODEGRADATION;

EID: 84908590359     PISSN: 1932104X     EISSN: 19321031     Source Type: Journal    
DOI: 10.1002/bbb.1467     Document Type: Review

References (67)

1. Kamm B and Kamm M, Biorefineries - Multi product processes, in White Biotechnology, Vol. 105, (Eds.: R. Ulber, D. Sell), Springer, Berlin (2007) pp. 175-204.
2. Ragauskas AJ, Williams CK, Davison BH, Britovsek G, Cairney J, Eckert CA et al., The path forward for biofuels and biomaterials. Science 311:484-489 (2006).
3. Fengel D and Wegener G, Wood: Chemistry, ultrastructure, reactions, De Gruyter, Berlin, 1984.
4. Koshijima T and Watanabe T, Association between lignin and carbohydrates in wood and other plant tissues, Springer, Berlin, 2003.
5. Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF et al., Lignins: Natural polymers from oxidative coupling of 4-hydroxyphenylpropanoids. Phytochem Rev 3:29-60 (2004).
6. Martínez AT, Ruiz-Dueñas FJ, Martínez MJ, del Río JC and Gutiérrez A, Enzymatic delignification of plant cell wall: from nature to mill. Curr Opin Biotechnol 20:348-357 (2009).
7. Martínez AT, Camarero S, Guillén F, Gutiérrez A, Muñoz C, Varela E et al., Progress in biopulping of non-woody materials:Chemical, enzymatic and ultrastructural aspects of wheat straw delignification with ligninolytic fungi from the genus Pleurotus. FEMS Microbiol Rev 13:265-274 (1994).
8. Martínez AT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillén F et al., Biodegradation of lignocellulosics:Microbiological, chemical and enzymatic aspects of fungal attack to lignin. Int Microbiol 8:195-204 (2005).
9. Barrasa JM, Camarero S, Martínez AT and Ruel K, Ultrastructural aspects of wheat straw degradation by Phanerochaete chrysosporium and Trametes versicolor. Appl Microbiol Biotechnol 43:766-770 (1995).
10. Camarero S, Barrasa JM, Pelayo M and Martínez AT, Evaluation of Pleurotus species for wheat-straw biopulping. J Pulp Paper Sci 24:197-203 (1998).
11. Salvachúa D, Prieto A, Lopez-Abelairas M, Lú-Chau T, Martínez AT and Martínez MJ, Fungal pretreatment: An alternative in second-generation ethanol from wheat straw. Bioresource Technol 102:7500-7506 (2011).
12. Salvachúa D, Prieto A, Vaquero ME, Martínez AT and Martínez MJ, Sugar recoveries from wheat straw following treatments with the fungus Irpex lacteus. Bioresource Technol 131:218-225 (2013).
13. Camarero S, Böckle B, Martínez MJ and Martínez AT, Manganese-mediated lignin degradation by Pleurotus pulmonarius. Appl Environ Microbiol 62:1070-1072 (1996).
14. Camarero S, Bocchini P, Galletti GC, Martínez MJ and Martínez AT, Compositional changes of wheat lignin by a fungal peroxidase analyzed by Pyrolysis-GC/MS. J Anal Appl Pyrolysis 58/59:413-423 (2001).
15. Camarero S, Sarkar S, Ruiz-Dueñas FJ, Martínez MJ and Martínez AT, Description of a versatile peroxidase involved in natural degradation of lignin that has both Mn-peroxidase and lignin-peroxidase substrate binding sites. J Biol Chem 274:10324-10330 (1999).
16. Camarero S, Ruiz-Dueñas FJ, Sarkar S, Martínez MJ and Martínez AT, The cloning of a new peroxidase found in lignocellulose cultures of Pleurotus eryngii and sequence comparison with other fungal peroxidases. FEMS Microbiol Lett 191:37-43 (2000).
17. Martínez MJ, Ruiz-Dueñas FJ, Guillén F and Martínez AT, Purification and catalytic properties of two manganeseperoxidase isoenzymes from Pleurotus eryngii. Eur J Biochem 237:424-432 (1996).
18. Ruiz-Dueñas FJ, Martínez MJ and Martínez AT, Molecular characterization of a novel peroxidase isolated from the ligninolytic fungus Pleurotus eryngii. Mol Microbiol 31:223-236 (1999).
19. Tien M and Kirk TK, Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium Burds. Science 221:661-663 (1983).
20. Gold MH, Kuwahara M, Chiu AA and Glenn JK, Purification and characterization of an extracellular H2O2-requiring diarylpropane oxygenase from the white rot basidiomycete Phanerochaete chrysosporium. Arch Biochem Biophys 234:353-362 (1984).
21. Kuwahara M, Glenn JK, Morgan MA and Gold MH, Separation and characterization of two extracellular H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett 169:247-250 (1984).
22. Ruiz-Dueñas FJ, Camarero S, Pérez-Boada M, Martínez MJ and Martínez AT, A new versatile peroxidase from Pleurotus. Biochem Soc Trans 29:116-122 (2001).
23. Ruiz-Dueñas FJ, Morales M, García E, Miki Y, Martínez MJ and Martínez AT, Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot 60:441-452 (2009).
24. Sugano Y, Muramatsu R, Ichiyanagi A, Sato T and Shoda M, DyP, a unique dye-decolorizing peroxidase, represents a novel heme peroxidase family. J Biol Chem 282:36652-36658 (2007).
25. Salvachúa D, Prieto A, Martínez AT and Martínez MJ, Characterization of a novel DyP-type peroxidase from Irpex lacteus and its application in the enzymatic hydrolysis of wheat straw. Appl Environ Microbiol 79:4316-4324 (2013).
26. Liers C, Bobeth C, Pecyna M, Ullrich R and Hofrichter M, DyPlike peroxidases of the jelly fungus Auricularia auricula-judae oxidize nonphenolic lignin model compounds and high-redox potential dyes. Appl Microbiol Biotechnol 85:1869-1879 (2010).
27. Salvachúa D, Martínez AT, Tien M, López-Lucendo MF, García F, de los Ríos V et al., Differential proteomic analysis of the secretome of Irpex lacteus and other white-rot fungi during wheat straw pretreatment. Biotechnol Biofuels 6:115 (2013).
28. Jurado M, Prieto A, Martínez-Alcalá MA, Martínez AT and Martínez MJ, Laccase detoxification of steam-exploded wheat straw for second generation bioethanol. Bioresource Technol 100:6378-6384 (2009).
29. Bourbonnais R and Paice MG, Oxidation of non-phenolic substrates. An expanded role for laccase in lignin biodegradation. FEBS Lett 267:99-102 (1990).
30. Sigoillot C, Camarero S, Vidal T, Record E, Asther M, Pérez-Boada M, Martínez MJ, Sigoillot J-C, Asther M, Colom J and Martínez AT, Comparison of different fungal enzymes for bleaching high-quality paper pulps. J Biotechnol 115:333-343 (2005).
31. García O, Camarero S, Colom J, Martínez AT, Martínez MJ, Monje R and Vidal T, Optimization of a laccase-mediator stage for TCF bleaching of flax pulp. Holzforschung 57:513-519 (2003).
32. Camarero S, García O, Vidal T, Colom J, del Río JC, Gutiérrez A, Gras JM, Monje R, Martínez MJ and Martínez AT, efficient bleaching of non-wood high-quality paper pulp using laccasemediator system. Enzyme Microb Technol 35:113-120 (2004).
33. Ibarra D, Romero J, Martínez MJ, Martínez AT and Camarero S, Exploring the enzymatic parameters for optimal delignification of eucalypt pulp by laccase-mediator. Enzyme Microb Technol 39:1319-1327 (2006).
34. Ibarra D, Camarero S, Romero J, Martínez MJ and Martínez AT, Integrating laccase-mediator treatment into an industrialtype sequence for totally chlorine free bleaching eucalypt kraft pulp. J Chem Technol Biotechnol 81:1159-1165 (2006).
35. Ibarra D, Chávez MI, Rencoret J, del Río JC, Gutiérrez A, Romero J, Camarero S, Martínez MJ, Jiménez-Barbero J and Martínez AT, Structural modification of eucalypt pulp lignin in a totally chlorine free bleaching sequence including a laccasemediator stage. Holzforschung 61:634-646 (2007).
36. Camarero S, Galletti GC and Martínez AT, Demonstration of in situ oxidative degradation of lignin side-chains by two white-rot fungi using analytical pyrolysis of methylated wheat straw. Rapid Commun Mass Spectrom 11:331-334 (1997).
37. Gutiérrez A, del Río JC, Ibarra D, Rencoret J, Romero J, Speranza M, Camarero S, Martínez MJ and Martínez AT, Enzymatic removal of free and conjugated sterols forming pitch deposits in environmentally sound bleaching of eucalypt paper pulp. Environ Sci Technol 40:3416-3422 (2006).
38. Speranza M, Ibarra D, Romero J, Martínez AT, Martínez MJ and Camarero S, Microscopy studies reveal delignification and sterol removal from eucalypt kraft pulps by laccase-HBT. Biocatal Biotransform 25:251-259 (2007).
39. Rodríguez E, Nuero O, Guillén F, Martínez AT and Martínez MJ, Degradation of phenolic and non-phenolic aromatic pollutants by four Pleurotus species: the role of laccase and versatile peroxidase. Soil Biol Biochem 36:909-916 (2004).
40. Camarero S, Ibarra D, Martínez MJ and Martínez AT, Ligninderived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol 71:1775-1784 (2005).
41. Cañas A, Alcalde M, Plou FJ, Martínez MJ, Martínez AT and Camarero S, Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environ Sci Technol 41:2964-2971 (2007).
42. Fillat U, Prieto A, Camarero S, Martínez AT and Martínez MJ, Biodeinking of flexographic inks by fungal laccases using synthetic and natural mediators. Biochem Eng J 67:97-103 (2012).
43. Kunamneni A, Camarero S, Garcia-Burgos C, Plou FJ, Ballesteros A and Alcalde M, Engineering and applications of fungal laccases for organic synthesis. Microb Cell Fact 7:32 (2008).
44. Widsten P and Kandelbauer A, Laccase applications in the forest products industry: A review. Enzyme Microb Technol 42:293-307 (2008).
45. Prasetyo EN, Kudanga T, Ostergaard L, Rencoret J, Gutiérrez A, del Río JC et al., Polymerization of lignosulfonates by the laccase-HBT (1-hydroxybenzotriazole) system improves dispersibility. Bioresource Technol 101:5054-5062 (2010).
46. Aracri E, Fillat A, Colom JF, Gutiérrez A, del Río JC, Martínez AT and Vidal T, Enzymatic grafting of simple phenols on flax and sisal pulp fibres using laccases. Bioresource Technol 101:8211-8216 (2010).
47. Camarero S, Galletti GC and Martínez AT, Preferential degradation of phenolic lignin-units by two white-rot fungi. Appl Environ Microbiol 60:4509-4516 (1994).
48. Martínez MJ, Muñoz C, Guillén F and Martínez AT, Studies on homoveratric acid transformation by the ligninolytic fungus Pleurotus eryngii. Appl Microbiol Biotechnol 41:500-504 (1994).
49. Cañas AI and Camarero S, Laccases and their natural mediators:Biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28:694-705 (2010).
50. Camarero S, Ibarra D, Martínez AT, Romero J, Gutiérrez A and del Río JC, Paper pulp delignification using laccase and natural mediators. Enzyme Microb Technol 40:1264-1271 (2007).
51. Camarero S, Cañas AI, Nousiainen P, Record E, Lomascolo A, Martínez MJ and Martínez AT, p-Hydroxycinnamic acids as natural mediators for laccase oxidation of recalcitrant compounds. Environ Sci Technol 42:6703-6709 (2008).
52. Gutiérrez A, Rencoret J, Ibarra D, Molina S, Camarero S, Romero J et al., Removal of lipophilic extractives from paper pulp by laccase and lignin-derived phenols as natural mediators. Environ Sci Technol 41:4124-4129 (2007).
53. Babot ED, Rico A, Rencoret J, Kalum L, Lund H, Romero J et al., Towards industrially feasible delignification and pitch removal by treating paper pulp with Myceliophthora thermophila laccase and a phenolic mediator. Bioresource Technol 102:6717-6722 (2011).
54. Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J et al., Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695-700 (2004).
55. Martinez D, Challacombe J, Morgenstern I, Hibbett DS, Schmoll M, Kubicek CP et al., Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci USA 106:1954-1959 (2009).
56. Fernández-Fueyo E, Ruiz-Dueñas FJ, Ferreira P, Floudas D, Hibbett DS, Canessa P et al., Comparative genomics of Ceriporiopisis subvermispora and Phanerochaete chrysosporium provide insight into selective ligninolysis. Proc Natl Acad Sci USA 109:5458-5463 (2012).
57. Fernández-Fueyo E, Ruiz-Dueñas FJ, Miki Y, Martínez MJ, Hammel KE and Martínez AT, Lignin-degrading peroxidases from genome of selective ligninolytic fungus Ceriporiopsis subvermispora. J Biol Chem 287:16903-16906 (2012).
58. Floudas D, Binder M, Riley R, Barry K, Blanchette RA, Henrissat B et al., The Paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science 336:1715-1719 (2012).
59. Ruiz-Dueñas FJ, Morales M, Pérez-Boada M, Choinowski T, Martínez MJ, Piontek K and Martínez AT, Manganese oxidation site in Pleurotus eryngii versatile peroxidase: A site-directed mutagenesis, kinetic and crystallographic study. Biochemistry 46:66-77 (2007).
60. Morales M, Mate MJ, Romero A, Martínez MJ, Martínez AT and Ruiz-Dueñas FJ, Two oxidation sites for low redoxpotential substrates: A directed mutagenesis, kinetic and crystallographic study on Pleurotus eryngii versatile peroxidase. J Biol Chem 287:41053-41067 (2012).
61. Ruiz-Dueñas FJ, Morales M, Rencoret J, Gutiérrez A, del Río JC, Martínez MJ and Martínez AT, Improved peroxidases. Patent (Spain) P200801292 (2008).
62. García-Ruiz E, González-Pérez D, Ruiz-Dueñas FJ, Martínez AT and Alcalde M, Directed evolution of a temperature-, peroxide- and alkaline pH-tolerant versatile peroxidase. Biochem J 441:487-498 (2012).
63. Maté D, García-Ruiz E, Camarero S and Alcalde M, Directed evolution of fungal laccases. Curr Genomics 12:113-122 (2011).
64. Maté D, García-Burgos C, García-Ruiz E, Ballesteros A, Camarero S and Alcalde M, Laboratory evolution of high redox potential laccases. Chem Biol 17:1030-1041 (2010).
65. Camarero S, Pardo I, Cañas AI, Molina P, Record E, Martínez AT, Martínez MJ and Alcalde M, Engineering platforms for directed evolution of laccase from Pycnoporus cinnabarinus. Appl Environ Microbiol 78:1370-1384 (2012).
66. Pardo I, Vicente AI, Alcalde M and Camarero S, Development of chimeric laccases by directed evolution. Biotechnol Bioeng 109:2978-2986 (2012).
67. Pardo I, Chanagá X, Vicente AI, Alcalde M and Camarero S., New colorimetric screening assays for the directed evolution of fungal laccases to improve the conversion of plant biomass. BMC Biotechnology 13:90 (2013).