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Comparative analysis of lignin peroxidase and manganese peroxidase activity on coniferous and deciduous wood using ToF-SIMS

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Abstract

White-rot fungi are distinguished by their ability to efficiently degrade lignin via lignin-modifying type II peroxidases, including manganese peroxidase (MnP) and lignin peroxidase (LiP). In the present study, time-of flight secondary ion mass spectrometry (ToF-SIMS) was used to evaluate lignin modification in three coniferous and three deciduous wood preparations following treatment with commercial preparations of LiP and MnP from two different white-rot fungi. Percent modification of lignin was calculated as a loss of intact methoxylated lignin over nonfunctionalized aromatic rings, which is consistent with oxidative cleavage of methoxy moieties within the lignin structure. Exposure to MnP resulted in greater modification of lignin in coniferous compared to deciduous wood (28 vs. 18 % modification of lignin); and greater modification of G-lignin compared to S-lignin within the deciduous wood samples (21 vs. 12 %). In contrast, exposure to LiP resulted in similar percent modification of lignin in all wood samples (21 vs 22 %), and of G- and S-lignin within the deciduous wood (22 vs. 23 %). These findings suggest that the selected MnP and LiP may particularly benefit delignification of coniferous and deciduous wood, respectively. Moreover, the current analysis further demonstrates the utility of ToF-SIMS for characterizing enzymatic modification of lignin in wood fibre along with potential advantages over UV and HPCL-MS detection of solubilized delignification products.

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References

  • Bajpai P, Anand A, Bajpai PK (2006) Bleaching with lignin-oxidizing enzymes. Biotechnol Annu Rev 12:349–378

    Article  CAS  PubMed  Google Scholar 

  • Baron CP, Bro R, Skibsted LH, Andersen HJ (1997) Direct measurement of lipid peroxidation in oil-in-water emulsions using multiwavelength derivative UV-spectroscopy. J Agric Food Chem 45:1741–1745. doi:10.1021/jf960638n

    Article  CAS  Google Scholar 

  • Bianco MA, Handaji A, Savolainen H (1998) Quantitative analysis of ellagic acid in hardwood samples. Sci Total Environ 222:123–126. doi:10.1016/S0048-9697(98)00294-0

    Article  CAS  Google Scholar 

  • Boeriu CG, Fitigau FI, Gosselink RJ, Frissen AE, Stoutjesdijk J, Peter F (2014) Fractionation of five technical lignins by selective extraction in green solvents and characterisation of isolated fractions. Ind Crop Prod 62:481–490. doi:10.1016/j.indcrop.2014.09.019

    Article  CAS  Google Scholar 

  • Boerjan W, Ralph J, Baucher M (2003) Lignin biosynthesis. Annu Rev Plant Biol 54:519–546. doi:10.1146/annurev.arplant.54.031902.134938

    Article  CAS  PubMed  Google Scholar 

  • Bonawitz ND, Chapple C (2010) The genetics of lignin biosynthesis: connecting genotype to phenotype. Annu Rev Genet 44:337–363. doi:10.1146/annurev-genet-102209-163508

    Article  CAS  PubMed  Google Scholar 

  • Campbell MM, Sederoff RR (1996) Variation in lignin content and composition. Plant Physiol 110:3–13

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen F, Dixon RA (2007) Lignin modification improves fermentable sugar yields for biofuel production. Nat Biotechnol 25:759–761. doi:10.1038/nbt1316

    Article  CAS  PubMed  Google Scholar 

  • Coconi-Linares N, Magaña-Ortíz D, Guzmán-Ortiz DA, Fernandez F, Loske AM, Gómez-Lim MA (2014) High-yield production of manganese peroxidase, lignin peroxidase, and versatile peroxidase in Phanerochaete chrysosporium. Appl Microbiol Biotechnol 98:9283–9294

    Article  CAS  PubMed  Google Scholar 

  • Conesa A, Punt PJ, van den Hondel CA (2002) Fungal peroxidases: molecular aspects and applications. J Biotechnol 93:143–158

    Article  CAS  PubMed  Google Scholar 

  • Cunha GGS, Masarin F, Norambuena M, Freer J, Ferraz A (2010) Linoleic acid peroxidation and lignin degradation by enzymes produced by Ceriporiopsis subvermispora grown on wood or in submerged liquid cultures. Enzym Microb Technol 46:262–267. doi:10.1016/j.enzmictec.2009.11.006

    Article  CAS  Google Scholar 

  • Faix O, Mozuch MD, Kirk TK (1985) Degradation of gymnosperm (guaiacyl) vs angiosperm (syringyl guaiacyl) lignins by Phanerochaete chrysosporium. Holzforschung 39:203–208. doi:10.1515/hfsg.1985.39.4.203

    Article  CAS  Google Scholar 

  • Fernández-Fueyo E, Ruiz-Dueñas FJ, Martínez AT (2014) Engineering a fungal peroxidase that degrades lignin at very acidic pH. Biotechnol Biofuels 7:114. doi:10.1186/1754-6834-7-114

    Article  PubMed  PubMed Central  Google Scholar 

  • Goacher RE, Edwards EA, Yakunin AF, Mims CA, Master ER (2012) Application of time-of-flight secondary ion mass spectrometry for the detection of enzyme activity on solid wood substrates. Anal Chem 84:4443–4451. doi:10.1021/ac3005346

    Article  CAS  PubMed  Google Scholar 

  • Goacher RE, Jeremic D, Master EM (2011) Expanding the library of secondary ions that distinguish lignin and polysaccharides in ToF-SIMS analysis of wood. Anal Chem 83:804–812. doi:10.1021/ac1023028

    Article  CAS  PubMed  Google Scholar 

  • Hakala TK, Maijala P, Konn J, Hatakka A (2004) Evaluation of novel wood-rotting polypores and corticioid fungi for the decay and biopulping of Norway spruce (Picea abies) wood. Enzyme Microb Tech 34:255–263. doi:10.1016/j.enzmictec.2003.10.014

    Article  CAS  Google Scholar 

  • Hammel KE, Cullen D (2008) Role of fungal peroxidases in biological ligninolysis. Curr Opin Plant Biol 11(3):349–355. doi:10.1016/j.pbi.2008.02.003

    Article  CAS  PubMed  Google Scholar 

  • Hammel KE, Tardone PJ, Moen MA, Price LA (1989) Biomimetic oxidation of nonphenolic lignin models by Mn(III): new observations on the oxidizability of guaiacyl and syringyl substructures. Arch Biochem Biophys 270:404–409. doi:10.1016/0003-9861(89)90044-1

    Article  CAS  PubMed  Google Scholar 

  • Henriksson G, Li J, Zhang L, Lindstrom ME (2010) Lignin utilization. RSC Energy Environ Series 2010:222–262

    Article  Google Scholar 

  • Hildén KS, Bortfeldt R, Hofrichter M, Hatakka A, Lundell TK (2008) Molecular characterization of the basidiomycete isolate Nematoloma frowardii b19 and its manganese peroxidase places the fungus in the corticioid genus Phlebia. Microbiology 514:2371–2379. doi:10.1099/mic.0.2008/018747-0

    Article  Google Scholar 

  • Hofrichter M, Lundell T, Hatakka A (2001) Conversion of milled pine wood by manganese peroxidase from Phlebia radiata. Appl Environ Microbiol 67:4588–4593. doi:10.1128/AEM.67.10.4588-4593.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hofrichter M, Ullrich R, Pecyna MJ, Liers C, Lundell T (2010) New and classic families of secreted fungal heme peroxidases. Appl Microbiol Biochem 87:871–897. doi:10.1007/s00253-010-2633-0

    Article  CAS  Google Scholar 

  • Holmbom B, Eckerman C, Eklund P, Hemming J, Nisula L, Reunanen M, Sjöholm R, Sundberg A, Sundberg K, Willför S (2003) Knots in trees: a new rich source of lignans. Phytochem Rev 2(3):331–340. doi:10.1023/B:PHYT.0000045493.95074.a8

    Article  CAS  Google Scholar 

  • Hori C, Gaskell J, Igarashi K, Samejima M, Hibbett D, Henrissat B, Cullen D (2013) Genomewide analysis of polysaccharides degrading enzymes in 11 white- and brown-rot Polyporales provides insight into mechanisms of wood decay. Mycologia 105(6):1412–1427. doi:10.3852/13-072

    Article  CAS  PubMed  Google Scholar 

  • Kapich A, Hofrichter M, Vares T, Hatakka A (1999) Coupling of manganese peroxidase-mediated lipid peroxidation with destruction of nonphenolic lignin model compounds and C-14-labeled lignins. Biochem Bioph Res Co 259:212–219. doi:10.1006/bbrc.1999.0742

    Article  CAS  Google Scholar 

  • Kapich AN, Korneichik TV, Hatakka A, Hammel KE (2010) Oxidizability of unsaturated fatty acids and of a non-phenolic lignin structure in the manganese peroxidase-dependent lipid peroxidation system. Enzyme Microb Tech 46:136–140. doi:10.1016/j.enzmictec.2009.09.014

    Article  CAS  Google Scholar 

  • Kersten P, Cullen D (2014) Copper radical oxidases and related extracellular oxidoreductases of wood-decay Agaricomycetes. Fungal Genet Biol 72:124–130. doi:10.1016/j.fgb.2014.05.011

    Article  CAS  PubMed  Google Scholar 

  • Lundell TK, Mäkelä MR, de Vries RP, Hildén KS (2014) Genomics, lifestyles and future prospects of wood-decay and litter-decomposing Basidiomycota. In: Martin FM (ed) Advances in Botanical Research 70:329–70. Academic Press, London

    Google Scholar 

  • Martínez AT, Speranza M, Ruiz-Dueñas FJ, Ferreira P, Camarero S, Guillén F, Martínez MJ, Gutiérrez A, del Río JC (2005) Biodegradation of lignocellulosics: microbiol, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204

    PubMed  Google Scholar 

  • Martínez AT, Ruiz-Dueñas FJ, Martínez MJ, Del Río JC, Gutiérrez A (2009) Enzymatic delignification of plant cell wall: from nature to mill. Curr Opin Biotechnol 20(3):348–357. doi:10.1016/j.copbio.2009.05.002

    Article  PubMed  Google Scholar 

  • Moreno AD, Ibarra D, Alvira P, Tomás-Pejó E, Ballesteros M (2015) A review of biological delignification and detoxification methods for lignocellulosic bioethanol production. Crit Rev Biotechnol 35:342–354. doi:10.3109/07388551.2013.878896

    Article  PubMed  Google Scholar 

  • Nousiainen P, Kontro J, Manner H, Hatakka A, Sipilä J (2014) Phenolic mediators enhance the manganese peroxidase catalyzed oxidation of recalcitrant lignin model compounds and synthetic lignin. Fungal Genet Biol 72:137–149. doi:10.1016/j.fgb.2014.07.008

    Article  CAS  PubMed  Google Scholar 

  • Otjen L, Blanchette RA (1988) Lignin distribution in wood delignified by white-rot fungi—X-ray microanalysis of decayed wood treated with bromine. Holzforschung 42:281–288. doi:10.1515/hfsg.1988.42.5.281

    Article  CAS  Google Scholar 

  • Petruzzi L, Bevilacqua A, Ciccarone C, Gambacorta G, Irlante G, Pati S, Sinigaglia M (2010) Use of microfungi in the treatment of oak chips: possible effects on wine. J Sci Food Agric 90:2617–2626. doi:10.1002/jsfa.4130

    Article  CAS  PubMed  Google Scholar 

  • Ralph J, Lundquist K, Brunow G, Lu F, Kim H, Schatz PF, Marita JM, Hatfield RD, Ralph SA, Christensen JH, Boerjan W (2004) Lignins: natural polymers from oxidative coupling of 4-hydroxyphenyl-propanoids. Phytochem Rev 3:29–60. doi:10.1023/B:PHYT.0000047809.65444.a4

    Article  CAS  Google Scholar 

  • Riley R, Salamov AA, Brown DW, Nagy LG, Floudas D, Held BW, Levasseur A, Lombard V, Morin E, Otillar R, Lindquist EA, Sun H, LaButti KM, Schmutz J, Jabbour D, Luo H, Baker SE, Pisabarro AG, Walton JD, Blanchette RA, Henrissat B, Martin F, Cullen D, Hibbett DS, Grigoriev IV (2014) Extensive sampling of basidiomycete genomes demonstrates inadequacy of the white-rot/brown-rot paradigm for wood decay fungi. Proc Natl Acad Sci U S A 111:9923–9928. doi:10.1073/pnas.1400592111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Dueñas FJ, Martínez AT (2009) Microbial degradation of lignin: how a bulky recalcitrant polymer is efficiently recycled in nature and how we can take advantage of this. Microb Biotechnol 2(2):164–177. doi:10.1111/j.1751-7915.2008.00078.x

    Article  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Duenas FJ, Lundell T, Floudas D, Nagy LG, Barrasa JM, Hibbett DS, Martinez AT (2013) Lignin-degrading peroxidases in Polyporales: an evolutionary survey based on 10 sequenced genomes. Mycologia 105:1428–1444. doi:10.3852/13-059

    Article  CAS  PubMed  Google Scholar 

  • Santos RB, Hart PW, Jameel H, Chang H (2013) Wood based lignin reactions important to the biorefinery and pulp and paper industries. Bioresources 8:1456–1477

    Google Scholar 

  • Silveira MHL, Morais ARC, Da Costa Lopes AM, Olekszyszen DN, Bogel-Łukasik R, Andreaus J, Pereira Ramos L (2015) Current pretreatment technologies for the development of cellulosic ethanol and biorefineries. ChemSusChem 8:3366–3390. doi:10.1002/cssc.201500282

    Article  CAS  PubMed  Google Scholar 

  • Sjöström E (1993) Wood chemistry: fundamentals and applications. Academic Press, San Diego

    Google Scholar 

  • Tolbert A, Akinosho H, Khunsupat R, Naskar AK, Ragauskas AJ (2014) Characterization and analysis of the molecular weight of lignin for biorefining studies. Biofuels Bioprod Bioref 8:836–856. doi:10.1002/bbb

    Article  CAS  Google Scholar 

  • Watanabe T, Tsuda S, Nishimura H, Honda Y, Watanabe T (2010) Characterization of a Δ12-fatty acid desaturase gene from Ceriporiopsis subvermispora, a selective lignin-degrading fungus. Appl Microbiol Biot 87:215–224. doi:10.1007/s00253-010-2438-1

    Article  CAS  Google Scholar 

  • Weng JK, Chapple C (2010) The origin and evolution of lignin biosynthesis. New Phytol 187:273–285. doi:10.1111/j.1469-8137.2010.03327.x

    Article  CAS  PubMed  Google Scholar 

  • Zhou C, Li Q, Chiang VL, Lucia LA, Griffis DP (2011) Chemical and spatial differentiation of syringyl and guaiacyl lignins in poplar wood via time-of-flight secondary ion mass spectrometry. Anal Chem 83:7020–7026. doi:10.1021/ac200903y

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Emma R. Master.

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This work was supported by grants from the Natural Sciences and Engineering Research Council and by the Government of Canada through Genome Canada and the Ontario Genomics Institute.

(Grant 2009-OGI-ABC-1405), as part of the Bioproducts and Enzymes from Environmental Metagenomes (BEEM) Project. The TOF-SIMS analyses were performed at Surface.

Interface Ontario, an analytical facility funded by the Canadian Foundation for Innovation (project no.11128), the Ontario Research Fund and institutional partners.

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The authors declare that they have no competing interests.

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MacDonald, J., Goacher, R.E., Abou-Zaid, M. et al. Comparative analysis of lignin peroxidase and manganese peroxidase activity on coniferous and deciduous wood using ToF-SIMS. Appl Microbiol Biotechnol 100, 8013–8020 (2016). https://doi.org/10.1007/s00253-016-7560-2

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  • DOI: https://doi.org/10.1007/s00253-016-7560-2

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