Open Access
Subscription Access
Insights into the Mechanism of Lignocellulose Degradation by Versatile Peroxidases
Lignocelluloses are imperative structural components of plant cell wall and are profusely found in agricultural crop residues. The structural heterogeneity and recalcitrance of lignin limit the accessibility of cell wall carbohydrates for constructive exploitation. During the past decades, diverse lignin degrading enzymes were characterized to facilitate the utilization of lignocellulosic biomass for technological applications. Versatile peroxidases are unique among ligninolytic enzymes for their remarkably high redox potential and ability to oxidize lignin without the requisite of redox mediators. The hybrid structural architecture of this enzyme bearing functional features of lignin peroxidase and manganese peroxidase demonstrates its versatility in aromatics oxidation. This review summarizes the distinctive structural aspects of fungal versatile peroxidase in correlation to its oxidation of aromatic substrates besides emphasizing on the catalytic environment conducive for substrate oxidation. This review also focuses on the general strategies employed for production of this enzyme, its molecular framework, potential biotechnological applications of versatile peroxidase and prospects on enhancing the production of enzyme. Finally, the significance of this enzyme in improving the nutritive value of crop residues to promote ruminal productivity is highlighted.
Keywords
Lignolytic Enzyme, Lignin Degradation, Ruminant Nutrition, White Rot Fungi.
User
Font Size
Information
- Kent, K. T., Enzymatic ‘combustion’, the microbial degradation of Lignin. Ann. Rev. Microbiol., 1987, 41, 465–505.
- Bugg, T. D. H., Ahmad, M., Hardiman, E. M. and Singh, R., The emerging role for bacteria in lignin degradation and bio-product formation. Curr. Opin. Biotech., 2011, 22, 394–400.
- Gonzalo, De G., Colpa, D. I., Habib, M. H. M. and Fraije, M. W., Bacterial enzymes involved in lignin degradation. J. Biotechnol., 2016, 236, 110–119.
- Mester, T. and Field, J. A., Characterization of a novel manganese peroxidase-lignin peroxidase hybrid isozyme produced by Bjerkandera species Strain BOS55 in the absence of manganese. J. Biol. Chem., 1998, 273, 15412–15417.
- Ruiz-Duenas, F. J., Morales, M., Garcia, E., Miki, Y., Martinez, M. J. and Martínez, A. T., Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J. Exp. Bot., 2009, 60, 441–452.
- Torres, E. and Ayala, M., Biocatalysis based on heme peroxidases: peroxidases as potential industrial biocatalysts. Springer Science and Business Media, Science, 2010, p. 358.
- Busse, N., Wagner, D., Kraume, M. and Czermak. P., Reaction kinetics of versatile peroxidase for degradation of lignin compounds. Am. J. Biochem. Biotechnol., 2013, 9(4), 365–394.
- Martinez, M. J., Ruiz-Duenas, F. J., Guillen, F. and Martinez, A. T., Purification and catalytic properties of two manganeseperoxidase isoenzymes from Pleurotus eryngii. Eur. J. Biochem., 1996, 237, 424–432.
- Harvey, P. J. and Palmer, J. M., Oxidation of phenolic compounds by ligninases. J. Biotechnol., 1990, 13, 169–179.
- Knop, D., Yarden, O. and Hadar, Y., The lignolytic peroxidases in the genus Pleurotus: divergence in activities, expression, and potential applications. Appl. Microbiol. Biotechnol., 2015, 99, 1025–1038.
- Palmer, J. M., Harvey, P. J. and Schoemaker, H. E., The role of peroxidases, radical cations and oxygen in the degradation of lignin (and Discussion). Philos. Trans. R. Soc. London A, 1987, 321, 495–505.
- Schoemaker, H. E., On the chemistry of lignin biodegradation. Rec. Travaux Chim. Pays-Bas., 1990, 109, 255–272.
- Guillen, F. and Evans, C. S., Anisaldehyde and veratraldehyde acting as redox cycling agents for H2O2 production by Pleurotus eryngii. Appl. Environ. Microbiol., 1994, 60, 2811–2817.
- Ruiz-Duenas, F. J. and Martinez, A. T., Structural and functional features of peroxidases with a potential as industrial biocatalysts. In Biocatalysts Based on Heme Peroxidases, Springer, 2010, pp. 37–59.
- Hammel, K. E. and Cullen, D., Role of fungal peroxidases in biological ligninolysis. Curr. Opin. Plant Biol., 2008, 11, 349–355.
- Mester, T. and Field, J. A., Characterization of a novel manganese peroxidase lignin peroxidase hybrid enzyme produced by Bjerkandera species strain BOS55 in the absence of manganese. J. Biol. Chem., 1998, 273, 15412–15417.
- Camarero, S., Sarkar, S., Ruiz-Duenas, F. J., Martinez, M. J. and Martinez, A. T., Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. J. Biol. Chem., 1999, 274, 10324–10330.
- Tsukihara, T., Honda, Y., Sakai, R., Watanabe, T. and Watanabe, T., Mechanism for oxidation of high-molecular-weight substrates by a fungal versatile peroxidase, MnP2. Appl. Environ. Microbiol., 2008, 74, 2873–2881.
- Pogni, R. et al., A tryptophan neutral radical in the oxidized state of versatile peroxidase from Pleurotus eryngii: a combined multifrequency EPR and density functional theory study. J. Biol. Chem., 2006, 281, 9517–9526.
- Ruiz-Duenas, F. J. et al., Protein radicals in fungal versatile peroxidase: catalytic tryptophan radical in both compound I and compound II and studies on W164Y, W164H and W164S variants. J. Biol. Chem., 2009, 284, 7986–7994.
- Rodakiewicz-Nowak, J., Jarosz-Wilkołazka, A. and Luterek, J., Catalytic activity of versatile peroxidase from Bjerkandera fumosa in aqueous solutions of water–miscible organic solvents. Appl. Catal., 2006, 308, 56–61.
- Jarosz-Wilkolazka, A., Luterek, J. and Olszewska, A., Catalytic activity of versatile peroxidase from Bjerkandera fumosa at different pH. Biocatal Biotransfor., 2008, 26(4), 280–287.
- Ruiz-Duenas, F. J., Camarero, S., Perez-Boada, M., Martinez, M. J. and Martínez, A. T., A new versatile peroxidase from Pleurotus. Biochem. Soc. T, 2001, 29, 116–122.
- Fernandez-Fueyo, E., Ruiz-Duenas, F. J., Martinez, M. J., Romero, A., Hammel, K. E., Medrano, F. J. and Martinez, A. T., Ligninolytic peroxidase genes in the oyster mushroom genome: heterologous expression, molecular structure, catalytic and stability properties and lignin-degrading ability. Biotechnol. Biofuels., 2014, 7, 2.
- Pradeep, V. and Sridhar, M., Laccases: the blue oxidases with immense scope for biotechnological exploitation, Everyman’s Science, 2013, XLVII(5).
- Floudas, D. et al., The paleozoic origin of enzymatic lignin decomposition reconstructed from 31 fungal genomes. Science, 2012, 336, 1715–1719.
- Pozdnyakova, N., Makarov, O., Chernyshova, M., Turkovskaya, O. and Jarosz-Wilkolazka, A., Versatile peroxidase of Bjerkandera fumosa: substrate and inhibitor specificity. Enzyme Microb. Technol., 2013, 52, 44–53.
- Nikiforova, S. V. et al., Chrysene bioconversion by the white rot fungus Pleurotus ostreatus D1. Microbiology, 2010, 79, 456–460.
- Heinfing, A., Ruiz-Dueñas, F. J., Martínez, M. J., Bergbauer, Matthias, Szewzyk, U. and Martínez, A. T., A study on reducing substrates of manganese-oxidizing peroxidases fom Pleurotus eryngii and Bjerkandera adusta. FEBS Lett., 1998, 428, 141–146.
- Linke, D., Leonhardt, R., Eisele, N., Petersen, L. M., Riemer, S., Nimtz, M. and Berger, R. G., Carotene-degrading activities from Bjerkandera adusta possess an application in detergent industries. Bioprocess Biosys. Eng., 2015, 38, 1191–1199.
- Marques, G., Gamelas, Jose, A. F., Ruiz-Duenas, F. J., Del Rio, Jose, C., Evtuguin, D. V., Martinez, A. T. and Gutierrez, A., Delignification of eucalypt kraft pulp with manganese-substituted polyoxometalate assisted by fungal versatile peroxidase. Bioresource Technol., 2010, 101, 5935–5940.
- Placido, J. and Capared, S., Ligninolytic enzymes: a biotechnological alternative for bioethanol production. Bioresources Bioprocess., 2015, 2, 23.
- Arora, D. S. and Sharma, R. K., Effect of different supplements on bioprocessing of wheat straw by Phlebia brevispora: changes in its chemical composition, in vitro digestibility and nutritional properties. Bioresource Technol., 2011, 102, 8085–8091.
- Tuyen, D. V., Phuong, H. N., Cone, J. W., Baars, J. J. P., Sonnenberg, A. S. M. and Hendriks, W. H., Effect of fungal treatments of fibrous agricultural by-products on chemical composition and in vitro rumen fermentation and methane production. Bioresour. Technol., 2013, 129, 256–263.
- Yu, H., Zhang, X., Song, L., Ke, J., Xu, C., Du, W. and Zhang, J., Evaluation of white-rot fungi-assisted alkaline/oxidative pretreatment of corn straw undergoing enzymatic hydrolysis by cellulose. J. Biosci. Bioeng., 2010, 110, 660–664.
- Zadrazil, F. and Puniya, A. K., Influence of carbon dioxide on lignin degradation and digestibility of lignocellulosics treated with Pleurotus sajor-caju. Int. Biodeter. Biodegr., 1994, 33, 237–244.
- Sridhar, M., Bhatta, R., Dhali, A., Kumar, V. P., Vandana, T. and Senani, S., In vitro evaluation of the effect of exogenous lignolytic enzymes on the nutritive value of Eleusine coracana (Ragi Straw). Adv. Appl. Res., 2014, 6(1), 45–52.
- Kumar, V. P., Naik, C. and Sridhar, M., Production, purification and characterization of novel laccase produced by Schizophyllum commune NI-07 with potential for delignification of crop residues. Appl. Biochem. Microbiol., 2015, 51(4), 432–441.
- Thammaiha, V., Ramya, G. R., Samanta, A. K., Senani, S. and Sridhar, M., Effect of lignin peroxidases obtained from white rot fungi in delignification of cereal crop residues for ruminant feeding: changes in chemical composition and in vitro digestibility. IOSR J. Agric. Vet. Sci., 2016, 9(9), 47–58.
- Tsukihara, T., Honda, Y., Sakai, R., Watanabe, T. and Watanabe, T., Exclusive overproduction of recombinant versatile peroxidase MnP2 by genetically modified white rot fungus Pleurotus ostreatus. J. Biotechnol., 2006, 126, 431–439.
- Ruiz-Duenas, F. J. et al., Site-directed mutagenesis of the catalytic tryptophan environment in Pleurotus eryngii versatile peroxidase. Biochemistry, 2008, 47, 1685–1695.
- Ruiz-Duenas, F. J., Martinez, M. J. and Martinez, A. T., Molecular characterization of a novel peroxidase isolated from the ligninolytic fungus Pleurotus eryngii. Mol. Microbiol., 1999, 31, 223–235.
- Hofrichter, M., Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol., 2002, 30(4), 454–466.
- Agosin, E., Tollier, M. T., Brillouet, J. M., Thivend, P. and Odier, E., Fungal pretreatment of wheat straw: effects on the biodegradability of cell walls, structural polysaccharides, lignin and phenolic acids by rumen microorganisms. J. Sci. Food Agric., 1986, 37, 97–106.
- Jalc, D., Zitnan, R. and Nerud, F., Effect of fungus-treated straw on ruminal fermentation in vitro. Anim. Feed Sci. Technol., 1994 46, 131–141.
- Jalc, D., Nerud, F. and Siroka, P., The effectiveness of biological treatment of wheat straw by white-rot fungi. Folia Microbiol., 1998, 43, 687–689.
- Tuyen, V. D., Cone, J. W., Baars, J. J. P., Sonnenberg, A. S. M. and Hendriks, W. H., Fungal strain and incubation period affect chemical composition and nutrient availability of wheat straw for rumen fermentation. Bioresource Technol., 2012, 111, 336–342.
- Shrivastava, B., Nandal, P., Sharma, A., Jain, K. K., Khasa, Y. P. and Das, T. K., Solid state bioconversion of wheat straw into digestible and nutritive ruminant feed by Ganoderma sp.rckk02. Bioresource Technol., 2012, 107, 347–351.
- Valmaseda, M., Almendros, G. and Martínez, A. T., Chemical transformation of wheat straw constituents after solid-state fermentation with selected lignocellulose-degrading fungi. Biomass Bioenerg., 1991, 1, 261–266.
- Adamovic, M., Grubic, G., Milenkovic, I., Jovanovic, R., Protic, R. and Sretenovic, L., The biodegradation of wheat straw by Pleurotus ostreatus mushrooms and its use in cattle feeding. Anim. Feed Sci. Technol., 1998, 71, 357–362.
- Bakshi, M. P. S., Gupta, V. K. and Langar, P. N., Acceptability and nutritive evaluation of Pleurotus harvested spent wheat straw in buffaloes. Agric. Waste, 1985, 13, 51–57.
- Fazaeli, H., Azizi, A. and Amile, M., Nutritive value index of treated wheat straw with Pleurotus fungi fed to sheep. Pak. J. Biol. Sci., 2006, 9, 2444–2449.
- Shrivastava, B., Thakur, S., Khasa, Y. P., Gupte, A., Puniya, A. K. and Kuhad, R. C., White-rot fungal conversion of wheat straw to energy rich cattle feed. Biodegradation, 2011, 22, 823–831.
- Streeter, C. L., Conway, K. E., Horn, G W. and Mader, T. L., Nutritional evaluation of wheat straw incubated with the edible mushroom. Pleurotus ostreatus. J. Anim. Sci., 1982, 54, 183–188.
- Tripathi, J. P. and Yadav, J. S., Optimization of solid substrate fermentation of wheat straw into animal feed by Pleurotus ostreatus – a pilot effort. Anim. Feed Sci. Technol., 1992, 37, 59–72.
- Tsang, L. J., Reid, I. D. and Coxworth, E. C., Delignification of wheat straw by Pleurotus spp. under mushroom growing conditions. Appl. Environ. Microbiol., 1987, 53, 1304–1306.
- Bisaria, R., Madan, M. and Vasudevan, P., Utilization of agro-residues as animal feed through Bioconversion. Bioresour. Technol., 1997, 59, 5–8.
- Calzada, J. F., Franco, L. F., de Arriola, M. C., Rolz, C. and Ortiz, M. A., Acceptability, body weight changes and digestibility of spent wheat straw after harvesting of Pleurotus sajor-caju. Biol. Waste, 1987, 22, 303–309.
- Liang, Y. S., Yuan, X. Z., Zeng, G. M., Hu, C. L., Zhong, H. and Huang, D. L., Biodelignification of rice straw by Phanerochaete chrysosporium in the presence of dirhamnolipid. Biodegradation, 2010, 21, 615–624.
- Rai, S. N., Walli, T. K. and Gupta, B. N., The chemical composition and nutritive value of rice straw after treatment with urea or Coprinus fimetarius in a solid state fermentation system. Anim. Feed Sci. Technol., 1989, 26, 81–92.
- Sharma, R. and Arora, D., Changes in biochemical constituents of paddy straw during degradation by white rot fungi and its impact on in vitro digestibility. J. Appl. Microbiol., 2010, 109, 679–686.
- Sridhar, M., Senani, S. and Bhatta, R., Production of proteases and lignolytic enzymes during solid state fermentation (SSF) of finger millet straw (Eleusine coracana). Indian J. Anim. Sci., 2011, 81(7), 723–729.
- Sridhar, M., Bhatta, R., Dhali, A., Saravanan, M., Vidya Pradeep and Vandana Thammaiah. Effect of exogenous lignolytic enzymetreated ragi straw on DM intake, digestibility, rumen fermentation and rumen enzymes in sheep. Indian J. Anim. Sci., 2015, 85(9), 1012–1016.
- Hassim, H. A., Lourenço, M., Goh, Y. M., Baars, J. J. P. and Fievez, V., Rumen degradation of oil palm fronds is improved through pre-digestion with white rot fungi but not through supplementation with yeast or enzymes. Can. J. Anim. Sci., 2012, 92, 79–87.
- Rahman, M. M., Lourenço, M., Hassim, H. A., Baars, J. J. P., Sonnenberg, A. S. M. and Cone, J. W., Improving ruminal degradability of oil palm fronds using white rot fungi. Anim. Feed Sci. Technol., 2011, 169, 157–166.
- Okano, K., Ohkoshi, N., Nishiyama, A., Usagawa, T. and Kitagawa, M., Improving the nutritive value of madake bamboo, Phyllostachys bambusoides, for ruminants by culturing with the whiterot fungus Ceriporiopsis subvermispora. Anim. Feed Sci. Technol., 2009, 152, 278–285.
- Misra, A. K., Mishra, A. S., Tripathi, M. K., Prasad, R., Vaithiyanathan, S. and Jakhmola, R. C., Optimization of solid state fermentation of mustard (Brassica campestris) straw for production of animal feed by white rot fungi (Ganoderma lucidum). AsianAust. J. Anim. Sci., 2007, 20(2), 208–213.
- Okano, K., Kitagawa, M., Sasaki, Y. and Watanabe, T., Conversion of Japanese red cedar (Cryptomeria japonica) into a feed for ruminants by white-rot basidiomycetes. Anim. Feed Sci. Technol., 2005, 120, 235–243.
- Asiegbu, F. O., Paterson, A. and Smith, J. E., The effects of co-fungal cultures and supplementation with carbohydrate adjuncts on lignin biodegradation and substrate digestibility. World J. Microbiol. Biotechnol., 1996, 12, 273–279.
- Mukherjee, R. and Nandi, B., Improvement of in vitro digestibility through biological treatment of water hyacinth biomass by two Pleurotus species. Int. Biodeter. Biodegr., 2004, 53, 7–12.
- Alemawor, F., Dzogbefia, V. P., Oldham, J. H. and Oddoye, E. O. K., Effect of Pleurotus ostreatus fermentation on cocoa pod husk composition: influence of fermentation period and Mn(2+) supplementation on the fermentation process. Afr. J. Biotechnol., 2009, 8, 1950–1958.
Abstract Views: 348
PDF Views: 128