Skip to main content

Advertisement

SpringerLink
Log in

Qualitative and Quantitative Methods for Isolation and Characterization of Lignin-Modifying Enzymes Secreted by Microorganisms

  • Published:
BioEnergy Research Aims and scope Submit manuscript

Abstract

Lignin is a polyphenolic biopolymer synthesized by plants, for providing strength and rigidity to the plant cellular structure. It is closely associated with other plant polysaccharides in the cell wall such as cellulose and hemicellulose, constituting the most abundant biopolymer on the earth’s surface. However, the complete utilization of it is being explored for the past few years. Various research groups around the world are trying to replace conventional fuels with the second-generation biofuels from lignocellulose. Several physical, chemical, and biological conversion methods have been developed for the separation and utilization of this biomass, as a result of which biological methods for lignocellulose conversion are considered to be cheap and environment-friendly. Microorganisms, especially fungi and bacteria, have been able to degrade the lignocellulose network and convert it to commercially important biofuels by secreting several intra- and extra-cellular enzymes. In the past few years, research has been conducted to isolate efficient lignin-degrading microorganisms, as separation of lignin from cellulosic biomass is considered as a major hurdle in biofuel and pulping industries. In this article, we extensively discuss different small- and large-scale methods developed for the isolation and characterization of lignin-degrading microorganisms. We have also comprehensively discussed about the qualitative and quantitative methods for the identification and characterization of the lignin-degrading and lignin-degrading auxiliary enzymes by comparing different methods based on their efficiency. This review can be used as a primer for understanding and selecting the most efficient method for isolation and characterization of lignin-degrading microorganisms and their enzymes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  1. Sattler SE, Funnell-Harris DL (2013) Modifying lignin to improve bioenergy feedstocks: strengthening the barrier against pathogens. Front Plant Sci 4:70. doi:10.3389/fpls.2013.00070

    Article  PubMed  PubMed Central  Google Scholar 

  2. Kumar P, Barrett DM, Delwiche MJ, Stroeve P (2009) Methods for pretreatment of lignocellulosic biomass for efficient hydrolysis and biofuel production. Ind Eng Chem Res 48(8):3713–3729

    Article  CAS  Google Scholar 

  3. Ragauskas AJ, Beckham GT, Biddy MJ, Chandra R, Chen F, Davis MF, Davison BH, Dixon RA, Gilna P, Keller M (2014) Lignin valorization: improving lignin processing in the biorefinery. Science 344(6185):1246843

    Article  PubMed  CAS  Google Scholar 

  4. Rinaldi R, Jastrzebski R, Clough MT, Ralph J, Kennema M, Bruijnincx PC, Weckhuysen BM (2016) Paving the way for lignin valorisation: recent advances in bioengineering, biorefining and catalysis. Angew Chem Int Ed Engl 55(29):8164–8215

    Article  CAS  PubMed  Google Scholar 

  5. Bugg TD, Ahmad M, Hardiman EM, Singh R (2011) The emerging role for bacteria in lignin degradation and bio-product formation. Curr Opin Biotechnol 22(3):394–400

    Article  CAS  PubMed  Google Scholar 

  6. Pollegioni L, Tonin F, Rosini E (2015) Lignin‐degrading enzymes. FEBS J 282(7):1190–1213

    Article  CAS  PubMed  Google Scholar 

  7. Kirk TK, Farrell RL (1987) Enzymatic “combustion”: the microbial degradation of lignin. Annu Rev Microbiol 41(1):465–501

    Article  CAS  PubMed  Google Scholar 

  8. Levasseur A, Piumi F, Coutinho PM, Rancurel C, Asther M, Delattre M, Henrissat B, Pontarotti P, Asther M, Record E (2008) FOLy: an integrated database for the classification and functional annotation of fungal oxidoreductases potentially involved in the degradation of lignin and related aromatic compounds. Fungal Genet Biol 45(5):638–645

    Article  CAS  PubMed  Google Scholar 

  9. Morii H, Nakamiya K, Kinoshita S (1995) Isolation of a lignin-decolorizing bacterium. J Ferment Bioeng 80(3):296–299

    Article  CAS  Google Scholar 

  10. Pfennig N, Lippert KD (1966) Über das vitamin B12-Bedürfnis phototropher Schwefelbakterien. Arch Mikrobiol 55(3):245–256

    Article  CAS  Google Scholar 

  11. Raj A, Reddy MK, Chandra R, Purohit HJ, Kapley A (2007) Biodegradation of kraft-lignin by Bacillus sp. isolated from sludge of pulp and paper mill. Biodegradation 18(6):783–792

    Article  CAS  PubMed  Google Scholar 

  12. Haq I, Kumar S, Kumari V, Singh SK, Raj A (2016) Evaluation of bioremediation potentiality of ligninolytic Serratia liquefaciens for detoxification of pulp and paper mill effluent. J Hazard Mater 305:190–199

    Article  CAS  PubMed  Google Scholar 

  13. Chakar FS, Ragauskas AJ (2004) Review of current and future softwood kraft lignin process chemistry. Ind Crop Prod 20(2):131–141

    Article  CAS  Google Scholar 

  14. Pointing S (2001) Feasibility of bioremediation by white-rot fungi. Appl Microbiol Biotechnol 57(1–2):20–33

    CAS  PubMed  Google Scholar 

  15. Cripps C, Bumpus JA, Aust S (1990) Biodegradation of azo and heterocyclic dyes by Phanerochaete chrysosporium. Appl Environ Microbiol 56(4):1114–1118

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Rodriguez E, Pickard MA, Vazquez-Duhalt R (1999) Industrial dye decolorization by laccases from ligninolytic fungi. Curr Microbiol 38(1):27–32

    Article  CAS  PubMed  Google Scholar 

  17. Abadulla E, Tzanov T, Costa S, Robra K-H, Cavaco-Paulo A, Gübitz GM (2000) Decolorization and detoxification of textile dyes with a laccase from Trametes hirsuta. Appl Environ Microbiol 66(8):3357–3362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Podgornik H, Poljanšek I, Perdih A (2001) Transformation of Indigo carmine by Phanerochaete chrysosporium ligninolytic enzymes. Enzym Microb Technol 29(2):166–172

    Article  CAS  Google Scholar 

  19. Spadaro JT, Gold MH, Renganathan V (1992) Degradation of azo dyes by the lignin-degrading fungus Phanerochaete chrysosporium. Appl Environ Microbiol 58(8):2397–2401

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Heinfling A, Bergbauer M, Szewzyk U (1997) Biodegradation of azo and phthalocyanine dyes by Trametes versicolor and Bjerkandera adusta. Appl Microbiol Biotechnol 48(2):261–266

    Article  CAS  Google Scholar 

  21. Levin L, Papinutti L, Forchiassin F (2004) Evaluation of Argentinean white rot fungi for their ability to produce lignin-modifying enzymes and decolorize industrial dyes. Bioresour Technol 94(2):169–176

    Article  CAS  PubMed  Google Scholar 

  22. Bandounas L, Wierckx NJ, de Winde JH, Ruijssenaars HJ (2011) Isolation and characterization of novel bacterial strains exhibiting ligninolytic potential. BMC Biotechnol 11(1):94

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pointing SB (1999) Qualitative methods for the determination of lignocellulolytic enzyme production by tropical fungi. Fungal Diversity 2:17–33

    Google Scholar 

  24. Sundman V, Nase L (1971) A simple plate test for direct visualization of biological lignin degradation. Paperi ja puu 2:67–71

    Google Scholar 

  25. Tekere M, Mswaka A, Zvauya R, Read J (2001) Growth, dye degradation and ligninolytic activity studies on Zimbabwean white rot fungi. Enzym Microb Technol 28(4):420–426

    Article  CAS  Google Scholar 

  26. Bavendamm W (1928) Über das Vorkommen und den Nachweis von Oxydasen bei holzzerstörenden Pilzen. Z Pflanzenkr Pflanzenschutz 38(9/10):257–276

    CAS  Google Scholar 

  27. Temp U, Eggert C, Eriksson K-EL (1998) A small-scale method for screening of lignin-degrading microorganisms. Appl Environ Microbiol 64(4):1548–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Eriksson K-EL, Blanchette R, Ander P (2012) Microbial and enzymatic degradation of wood and wood components. Springer Science & Business Media, Berlin Heidelberg

    Google Scholar 

  29. Haider K, Trojanowski J (1975) Decomposition of specifically 14C-labelled phenols and dehydropolymers of coniferyl alcohol as models for lignin degradation by soft and white rot fungi. Arch Microbiol 105(1):33–41

    Article  CAS  Google Scholar 

  30. Rajan JS, Srinivasan V (1992) A colorimetric assay for lignin based on its reaction with diazotized sulfanilic acid and its use in studies on lignin biodegradation by bacteria. Biotechnol Tech 6(3):219–222

    Article  CAS  Google Scholar 

  31. Ahmad M, Taylor CR, Pink D, Burton K, Eastwood D, Bending GD, Bugg TD (2010) Development of novel assays for lignin degradation: comparative analysis of bacterial and fungal lignin degraders. Mol Biosyst 6(5):815–821

    Article  CAS  PubMed  Google Scholar 

  32. Zimmermann W, Paterson A, Broda P (1988) Conventional and high-performance size-exclusion chromatography of graminaceous lignin–carbohydrate complexes. Methods Enzymol 161:191–199

    Article  CAS  Google Scholar 

  33. McAuliffe L, Ellis RJ, Lawes JR, Ayling RD, Nicholas RA (2005) 16S rDNA PCR and denaturing gradient gel electrophoresis; a single generic test for detecting and differentiating Mycoplasma species. J Med Microbiol 54(8):731–739

    Article  CAS  PubMed  Google Scholar 

  34. Muyzer G, Smalla K (1998) Application of denaturing gradient gel electrophoresis (DGGE) and temperature gradient gel electrophoresis (TGGE) in microbial ecology. Antonie Van Leeuwenhoek 73(1):127–141

    Article  CAS  PubMed  Google Scholar 

  35. Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16S rRNA. Appl Environ Microbiol 59(3):695–700

    CAS  PubMed  PubMed Central  Google Scholar 

  36. Sheffield VC, Cox DR, Lerman LS, Myers RM (1989) Attachment of a 40-base-pair G+ C-rich sequence (GC-clamp) to genomic DNA fragments by the polymerase chain reaction results in improved detection of single-base changes. Proc Natl Acad Sci 86(1):232–236

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Niku-Paavola M, Raaska L, Itävaara M (1990) Detection of white-rot fungi by a non-toxic stain. Mycol Res 94(1):27–31

    Article  Google Scholar 

  38. Thurston CF (1994) The structure and function of fungal laccases. Microbiology 140(1):19–26

    Article  CAS  Google Scholar 

  39. Soden D, O’callaghan J, Dobson A (2002) Molecular cloning of a laccase isozyme gene from Pleurotus sajor-caju and expression in the heterologous Pichia pastoris host. Microbiology 148(12):4003–4014

    Article  CAS  PubMed  Google Scholar 

  40. Harkin JM, Larsen MJ, Obst JR (1974) Use of syringaldazine for detection of laccase in sporophores of wood rotting fungi. Mycologia 66:469–476

    Article  CAS  PubMed  Google Scholar 

  41. Duffey S, Aldrich J, Blum M (1977) Biosynthesis of phenol and guaiacol by the hemipteran Leptoglossus phyllopus. Comp Biochem Physiol B 56(2):101–102

    CAS  PubMed  Google Scholar 

  42. Dorfner R, Ferge T, Kettrup A, Zimmermann R, Yeretzian C (2003) Real-time monitoring of 4-vinylguaiacol, guaiacol, and phenol during coffee roasting by resonant laser ionization time-of-flight mass spectrometry. J Agric Food Chem 51(19):5768–5773

    Article  CAS  PubMed  Google Scholar 

  43. Sheikhi F, Ardakani MR, Enayatizamir N, Rodriguez-Couto S (2012) The determination of assay for laccase of Bacillus subtilis WPI with two classes of chemical compounds as substrates. Indian J Microbiol 52(4):701–707

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Kiiskinen LL, Rättö M, Kruus K (2004) Screening for novel laccase‐producing microbes. J Appl Microbiol 97(3):640–646

    Article  CAS  PubMed  Google Scholar 

  45. López M, Guisado G, Vargas-García M, Suárez-Estrella F, Moreno J (2006) Decolorization of industrial dyes by ligninolytic microorganisms isolated from composting environment. Enzym Microb Technol 40(1):42–45

    Article  CAS  Google Scholar 

  46. Childs RE, Bardsley WG (1975) The steady-state kinetics of peroxidase with 2, 2′-azino-di-(3-ethyl-benzthiazoline-6-sulphonic acid) as chromogen. Biochem J 145:93–103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Johannes C, Majcherczyk A (2000) Laccase activity tests and laccase inhibitors. J Biotechnol 78(2):193–199

    Article  CAS  PubMed  Google Scholar 

  48. Heinzkill M, Bech L, Halkier T, Schneider P, Anke T (1998) Characterization of laccases and peroxidases from wood-rotting fungi (family Coprinaceae). Appl Environ Microbiol 64(5):1601–1606

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Edens WA, Goins TQ, Dooley D, Henson JM (1999) Purification and characterization of a secreted laccase of Gaeumannomyces graminis var. tritici. Appl Environ Microbiol 65(7):3071–3074

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Prillinger H, Esser K (1977) The phenoloxidases of the ascomycete Podospora anserina. Mol Gen Genet 156(3):333–345

    Article  CAS  PubMed  Google Scholar 

  51. Harkin JM, Obst JR (1973) Syringaldazine, an effective reagent for detecting laccase and peroxidase in fungi. Experientia 29(4):381–387

    Article  CAS  Google Scholar 

  52. Dedeyan B, Klonowska A, Tagger S, Tron T, Iacazio G, Gil G, Le Petit J (2000) Biochemical and molecular characterization of a laccase from Marasmius quercophilus. Appl Environ Microbiol 66(3):925–929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Collins PJ, Kotterman M, Field JA, Dobson A (1996) Oxidation of Anthracene and Benzo[a]pyrene by Laccases from Trametes versicolor. Appl Environ Microbiol 62(12):4563–4567

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Johannes C, Majcherczyk A, Hüttermann A (1996) Degradation of anthracene by laccase of Trametes versicolor in the presence of different mediator compounds. Appl Microbiol Biotechnol 46(3):313–317

    Article  CAS  PubMed  Google Scholar 

  55. Majcherczyk A, Johannes C, Hüttermann A (1998) Oxidation of polycyclic aromatic hydrocarbons (PAH) by laccase of Trametes versicolor. Enzym Microb Technol 22(5):335–341

    Article  CAS  Google Scholar 

  56. Johannes C, Majcherczyk A, Hüttermann A (1998) Oxidation of acenaphthene and acenaphthylene by laccase of Trametes versicolor in a laccase-mediator system. J Biotechnol 61(2):151–156

    Article  CAS  Google Scholar 

  57. Pickard MA, Roman R, Tinoco R, Vazquez-Duhalt R (1999) Polycyclic aromatic hydrocarbon metabolism by white rot fungi and oxidation by Coriolopsis gallica UAMH 8260 laccase. Appl Environ Microbiol 65(9):3805–3809

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Alcalde M, Bulter T (2003) Colorimetric assays for screening laccases. In: Arnold FH, Giorgiu G (eds.) Directed enzyme evolution. Springer, Berlin Heidelberg, pp 193–201

  59. Glenn JK, Gold MH (1983) Decolorization of several polymeric dyes by the lignin-degrading basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 45(6):1741–1747

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Gold MH, Glenn JK, Alic M (1988). Use of polymericdyes in lignin biodegradation assays. Methods Enzymol161:74–78

  61. Xu F (1996) Catalysis of novel enzymatic iodide oxidation by fungal laccase. Appl Biochem Biotechnol 59(3):221–230

    Article  CAS  Google Scholar 

  62. Gabler M, Hensel M, Fischer L (2000) Detection and substrate selectivity of new microbial D-amino acid oxidases. Enzym Microb Technol 27(8):605–611

    Article  CAS  Google Scholar 

  63. Lonergan G, Baker W (1995) Comparative study of substrates of fungal laccase. Lett Appl Microbiol 21(1):31–33

    Article  CAS  Google Scholar 

  64. Boominathan K, Reddy C, Arora D, Elander R, Mukerji K (1992) Handbook of applied mycology. Marcel Dekker, New York

    Google Scholar 

  65. Pointing S, Vrijmoed L, Jones E (1999) Laccase is produced as the sole lignin-modifying enzyme in submerged liquid culture by the white-rot fungus Pycnoporus sanguineus L. Mycologia 91:345–349

    Google Scholar 

  66. Pointing S, Vrijmoed L, Jones E (1998) A qualitative assessment of lignocellulose degrading enzyme activity in marine fungi. Bot Mar 41(1–6):293–298

    Article  CAS  Google Scholar 

  67. Archibald FS (1992) A new assay for lignin-type peroxidases employing the dye azure B. Appl Environ Microbiol 58(9):3110–3116

    CAS  PubMed  PubMed Central  Google Scholar 

  68. Magalhães DB, de Carvalho MEA, Bon E, Neto JSA, Kling SH (1996) Colorimetric assay for lignin peroxidase activity determination using methylene blue as substrate. Biotechnol Tech 10(4):273–276

    Article  Google Scholar 

  69. Brown JA, Li D, Alic M, Gold MH (1993) Heat shock induction of manganese peroxidase gene transcription in Phanerochaete chrysosporium. Appl Environ Microbiol 59(12):4295–4299

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Arora DS, Gill PK (2001) Comparison of two assay procedures for lignin peroxidase. Enzym Microb Technol 28(7):602–605

    Article  CAS  Google Scholar 

  71. Tariq V-N, Irvine W (1995) Ligninolytic enzyme activity: a comparison of the veratryl alcohol and Azure B assay systems. Biotechnol Tech 9(3):197–202

    Article  CAS  Google Scholar 

  72. Paszczyński A, Crawford RL, Huynh V-B (1988) Manganese peroxidase of Phanerochaete chrysosporium: purification. Methods Enzymol 161C:264–270

    Article  Google Scholar 

  73. Vares T, Kalsi M, Hatakka A (1995) Lignin peroxidases, manganese peroxidases, and other ligninolytic enzymes produced by phlebia radiata during solid-state fermentation of wheat straw. Appl Environ Microbiol 61(10):3515–3520

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Orth AB, Royse D, Tien M (1993) Ubiquity of lignin-degrading peroxidases among various wood-degrading fungi. Appl Environ Microbiol 59(12):4017–4023

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Paszczyński A, Huynh V-B, Crawford R (1985) Enzymatic activities of an extracellular, manganese-dependent peroxidase from Phanerochaete chrysosporium. FEMS Microbiol Lett 29(1–2):37–41

    Article  Google Scholar 

  76. Martinez MJ, Ruiz-Duenas FJ, Guillen F, Martinez AT (1996) Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus eryngii. Eur J Biochem 237(2):424–432

    Article  CAS  PubMed  Google Scholar 

  77. Vasilchenko LG, Ludwig R, Yershevich OP, Haltrich D, Rabinovich ML (2012) High‐throughput screening for cellobiose dehydrogenases by Prussian Blue in situ formation. Biotechnol J 7(7):919–930

    Article  CAS  PubMed  Google Scholar 

  78. Kremer SM, Wood PM (1992) Evidence that cellobiose oxidase from Phanerochaete chrysosporium is primarily an Fe (III) reductas. Eur J Biochem 205(1):133–138

    Article  CAS  PubMed  Google Scholar 

  79. Baminger U, Subramaniam SS, Renganathan V, Haltrich D (2001) Purification and characterization of cellobiose dehydrogenase from the plant pathogen Sclerotium (Athelia) rolfsii. Appl Environ Microbiol 67(4):1766–1774

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Baminger U, Nidetzky B, Kulbe KD, Haltrich D (1999) A simple assay for measuring cellobiose dehydrogenase activity in the presence of laccase. J Microbiol Methods 35(3):253–259

    Article  CAS  PubMed  Google Scholar 

  81. Henriksson G, Polk V, Eriksson K-E (1997) Assay for cellobiose dehydrogenase in the presence of laccase. Biotechnol Tech 11(10):743–745

    Article  CAS  Google Scholar 

  82. Guillen F, Martinez AT, Martinez MJ (1992) Substrate specificity and properties of the aryl‐alcohol oxidase from the ligninolytic fungus Pleurotus eryngii. Eur J Biochem 209(2):603–611

    Article  CAS  PubMed  Google Scholar 

  83. Gutierrez A, Caramelo L, Prieto A, Martínez MJ, Martinez AT (1994) Anisaldehyde production and aryl-alcohol oxidase and dehydrogenase activities in ligninolytic fungi of the genus Pleurotus. Appl Environ Microbiol 60(6):1783–1788

    CAS  PubMed  PubMed Central  Google Scholar 

  84. Ruiz-Dueñas FJ, Ferreira P, Martínez MJ, Martínez AT (2006) In vitro activation, purification, and characterization of Escherichia coli expressed aryl-alcohol oxidase, a unique H 2 O 2-producing enzyme. Protein Expr Purif 45(1):191–199

    Article  PubMed  CAS  Google Scholar 

  85. Ferreira P, Hernández-Ortega A, Herguedas B, Rencoret J, Gutiérrez A, Martinez M, Jiménez-Barbero J, Medina M (2010) Kinetic and chemical characterization of aldehyde oxidation by fungal aryl-alcohol oxidase. Biochem J 425:585–593

    Article  CAS  PubMed  Google Scholar 

  86. Tamboli DP, Telke AA, Dawkar VV, Jadhav SB, Govindwar SP (2011) Purification and characterization of bacterial aryl alcohol oxidase from Sphingobacterium sp. ATM and its uses in textile dye decolorization. Biotechnol Bioprocess Eng 16(4):661–668

    Article  CAS  Google Scholar 

  87. Feldman D, Kowbel DJ, Glass NL, Yarden O, Hadar Y (2015) Detoxification of 5-hydroxymethylfurfural by the Pleurotus ostreatus lignolytic enzymes aryl alcohol oxidase and dehydrogenase. Biotechnol Biofuels 8(1):63

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  88. Ferreira P, Medina M, Guillén F, Martinez M, Van Berkel W, Martinez A (2005) Spectral and catalytic properties of aryl-alcohol oxidase, a fungal flavoenzyme acting on polyunsaturated alcohols. Biochem J 389:731–738

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Danneel HJ, Rossner E, Zeeck A, Giffhorn F (1993) Purification and characterization of a pyranose oxidase from the basidiomycete Peniophora gigantea and chemical analyses of its reaction products. Eur J Biochem 214(3):795–802

    Article  CAS  PubMed  Google Scholar 

  90. Furukawa H, Wieser M, Morita H, Sugio T, Nagasawa T (1999) Purification and characterization of vanillyl-alcohol oxidase from Byssochlamys fulva V107. J Biosci Bioeng 87(3):285–290

    Article  CAS  PubMed  Google Scholar 

  91. Fraaije MW, Veeger C, van Berkel WJ (1995) Substrate specificity of flavin-dependent vanillyl-alcohol oxidase from Penicillium simplicissimum. Eur J Biochem 234:271–277

    Article  CAS  PubMed  Google Scholar 

  92. Jong E, Berkel WJ, Zwan RP, Bont JA (1992) Purification and characterization of vanillyl‐alcohol oxidase from Penicillium simplicissimum. Eur J Biochem 208(3):651–657

    Article  PubMed  Google Scholar 

  93. Fraaije MW, Pikkemaat M, Van Berkel W (1997) Enigmatic gratuitous induction of the covalent flavoprotein vanillyl-alcohol oxidase in Penicillium simplicissimum. Appl Environ Microbiol 63(2):435–439

    CAS  PubMed  PubMed Central  Google Scholar 

  94. van den Heuvel RH, van den Berg WA, Rovida S, van Berkel WJ (2004) Laboratory-evolved vanillyl-alcohol oxidase produces natural vanillin. J Biol Chem 279(32):33492–33500

    Article  PubMed  CAS  Google Scholar 

  95. Kersten PJ, Kirk TK (1987) Involvement of a new enzyme, glyoxal oxidase, in extracellular H2O2 production by Phanerochaete chrysosporium. J Bacteriol 169(5):2195–2201

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Kersten PJ (1990) Glyoxal oxidase of Phanerochaete chrysosporium: its characterization and activation by lignin peroxidase. Proc Natl Acad Sci 87(8):2936–2940

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Brugger D, Krondorfer I, Shelswell C, Huber-Dittes B, Haltrich D, Peterbauer CK (2014) Engineering pyranose 2-oxidase for modified oxygen reactivity. PLoS One 8(9):e109242

    Article  CAS  Google Scholar 

  98. Baron AJ, Stevens C, Wilmot C, Seneviratne KD, Blakeley V, Dooley DM, Phillips S, Knowles PF, McPherson MJ (1994) Structure and mechanism of galactose oxidase. The free radical site. J Biol Chem 269(40):25095–25105

    CAS  PubMed  Google Scholar 

  99. Raba J, Mottola HA (1995) Glucose oxidase as an analytical reagent. Crit Rev Anal Chem 25(1):1–42

    Article  CAS  Google Scholar 

  100. Dobrick LA (1958) Screening method for glucose of blood serum utilizing glucose oxidase and an indophenol indicator. J Biol Chem 231(1):403–409

    CAS  PubMed  Google Scholar 

  101. Salomon L, Johnson JE (1959) Enzymatic microdetermination of glucose in blood and urine. Anal Chem 31(3):453–456

    Article  CAS  Google Scholar 

  102. Morley G, Dawson A, Marks V (1968) Manual and autoanalyzer methods for measuring blood glucose using guaiacum and glucose oxidase. Assoc Clin Biochem Proc 5(2):42–45

    Article  Google Scholar 

  103. Trinder P (1969) Determination of blood glucose using an oxidase-peroxidase system with a non-carcinogenic chromogen. J Clin Pathol 22(2):158–161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Werner W, Rey H-G, Wielinger H (1970) Über die Eigenschaften eines neuen Chromogens für die Blutzuckerbestimmung nach der GOD/POD-Methode. Fresenius’ Z Anal Chem 252(2–3):224–228

    Article  CAS  Google Scholar 

  105. Kabasakalian P, Kalliney S, Westcott A (1974) Enzymatic blood glucose determination by colorimetry of N, N-diethylaniline-4-aminoantipyrine. Clin Chem 20(5):606–607

    CAS  PubMed  Google Scholar 

  106. Clapp PA, Evans DF (1991) Spectrophotometric determination of hydrogen peroxide with leuco Patent Blue Violet. Anal Chim Acta 243:217–220

    Article  CAS  Google Scholar 

  107. Bateman RC Jr, Evans JA (1995) Using the glucose oxidase/peroxidase system in enzyme kinetics. J Chem Educ 72(12):A240

    Article  CAS  Google Scholar 

  108. Betancor L, López-Gallego F, Hidalgo A, Alonso-Morales N, Dellamora-Ortiz G, Guisán JM, Fernández-Lafuente R (2006) Preparation of a very stable immobilized biocatalyst of glucose oxidase from Aspergillus niger. J Biotechnol 121(2):284–289

    Article  CAS  PubMed  Google Scholar 

  109. Guilbault GG, Brignac PJ Jr, Zimmer M (1968) Homovanillic acid as a fluorometric substrate for oxidative enzymes. Analytical applications of the peroxidase, glucose oxidase, and xanthine oxidase systems. Anal Chem 40(1):190–196

    Article  CAS  PubMed  Google Scholar 

  110. Brock BJ, Rieble S, Gold MH (1995) Purification and characterization of a 1, 4-benzoquinone reductase from the basidiomycete Phanerochaete chrysosporium. Appl Environ Microbiol 61(8):3076–3081

    CAS  PubMed  PubMed Central  Google Scholar 

  111. Kim K (2002) Characterization of 1, 4-benzoquinone reductase from bovine liver. Biotechnol Bioprocess Eng 7(4):216–220

    Article  CAS  Google Scholar 

  112. Constam D, Muheim A, Zimmermann W, Fiechter A (1991) Purification and partial characterization of an intracellular NADH: quinone oxidoreductase from Phanerochaete chrysosporium. J Gen Microbiol 137(9):2209–2214

    Article  CAS  Google Scholar 

  113. Rehman AU, Thurston CF (1992) Purification of laccase I from Armillaria mellea. Microbiology 138(6):1251–1257

    Google Scholar 

  114. Yadav M, Yadav P, Yadav KDS (2009) Purification and characterization of lignin peroxidase from Loweporus lividus MTCC‐1178. Eng Life Sci 9(2):124–129

    Article  CAS  Google Scholar 

  115. Cheng X, Jia R, Li P, Tu S, Zhu Q, Tang W, Li X (2007) Purification of a new manganese peroxidase of the white-rot fungus Schizophyllum sp. F17, and decolorization of azo dyes by the enzyme. Enzym Microb Technol 41(3):258–264

    Article  CAS  Google Scholar 

  116. Asada Y, Watanabe A, Ohtsu Y, Kuwahara M (1995) Purification and characterization of an aryl-alcohol oxidase from the lignin-degrading basidiomycete Phanerochaete chrysosporium. Biosci Biotechnol Biochem 59(7):1339–1341

    Article  CAS  Google Scholar 

  117. Leitner C, Volc J, Haltrich D (2001) Purification and characterization of pyranose oxidase from the white rot fungus Trametes multicolor. Appl Environ Microbiol 67(8):3636–3644

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Paukner R, Staudigl P, Choosri W, Haltrich D, Leitner C (2015) Expression, purification, and characterization of galactose oxidase of Fusarium sambucinum in E. coli. Protein Expr Purif 108:73–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Swoboda BE, Massey V (1965) Purification and properties of the glucose oxidase from Aspergillus niger. J Biol Chem 240(5):2209–2215

    CAS  PubMed  Google Scholar 

  120. Martinez D, Larrondo LF, Putnam N, Gelpke MDS, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22(6):695–700

    Article  CAS  PubMed  Google Scholar 

  121. Martinez D, Challacombe J, Morgenstern I, Hibbett D, Schmoll M, Kubicek CP, Ferreira P, Ruiz-Duenas FJ, Martinez AT, Kersten P (2009) Genome, transcriptome, and secretome analysis of wood decay fungus Postia placenta supports unique mechanisms of lignocellulose conversion. Proc Natl Acad Sci 106(6):1954–1959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Kameshwar AkS QW (2016) Recent developments in using advanced sequencing technologies for the genomic studies of lignin and cellulose degrading microorganisms. Int J Biol Sci 12(2):156–171

    Article  CAS  Google Scholar 

  123. Ohm RA, Riley R, Salamov A, Min B, Choi I-G, Grigoriev IV (2014) Genomics of wood-degrading fungi. Fungal Genet Biol 72:82–90

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by NSERC-RDF fund to Wensheng Qin and Ontario Trillium Scholarship (OTS) to Ayyappa Kumar Sista Kameshwar.

Author information

Authors and Affiliations

  1. Department of Biology, Lakehead University, 955 Oliver Road, Thunder Bay, Ontario, P7B 5E1, Canada

    Ayyappa Kumar Sista Kameshwar & Wensheng Qin

Authors
  1. Ayyappa Kumar Sista Kameshwar
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wensheng Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wensheng Qin.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kameshwar, A.K.S., Qin, W. Qualitative and Quantitative Methods for Isolation and Characterization of Lignin-Modifying Enzymes Secreted by Microorganisms. Bioenerg. Res. 10, 248–266 (2017). https://doi.org/10.1007/s12155-016-9784-5

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12155-016-9784-5

Keywords

Search

Navigation