Determination of Pleurotus abieticola ligninolytic activity on Norway spruce wood

Abstract

The effect of Phlebiopsis gigantea treatment in control of Heterobasidion parviporum in Norway spruce is less effective than that in control of Heterobasidion annosum in pine. It is necessary to apply other fungi, for example, Pleurotus abieticola in Norway spruce stands. Thus, it is necessary to assess the activity of major ligninolytic enzymes, that is, laccase, lignin peroxidase (LiP), manganese peroxidase (MnP) and versatile peroxidase (VP) produced by P. abieticola, which may be effective in the fast degradation of Norway spruce wood. Three strains of P. abieticola (Pa1-3) were grown on pieces of Norway spruce sapwood and heartwood for 50 days in laboratory conditions. Enzymatic activity was determined using spectrophotometry. Pleurotus abieticola produced laccase, LiP, MnP and VP. The activity of laccase was low, ranging 0–3.696 and 0–0.806 mU/μg of protein in sapwood and heartwood, respectively. The highest activity in Pa1 = 3.696 mU/μg of protein in sapwood and in Pa3 = 0.806 mU/μg of protein in heartwood was observed after 30 and 50 days of incubation, respectively. The activity of LiP was also low, ranging 0–0.188 and 0–0.271 mU/μg of protein in sapwood and heartwood, respectively. The highest activity in Pa1 = 0.271 mU/μg of protein in sapwood and in Pa2 = 0.188 mU/μg of protein in heartwood was observed after 40 and 20 days of incubation, respectively. The activity of MnP ranged 0–17.618 and 0–12.203 mU/μg of protein in sapwood and heartwood, respectively. This enzymatic activity peaked at the 50th day of culture on sapwood for the Pa3 strain (17.618 mU/μg of protein) and at the 20th day of culture on heartwood for the Pa1 strain (12.203 mU/μg of protein). The activity of VP with manganese-oxidising properties was found to be high in all strains of P. abieticola, ranging 0–39.19 and 0–59.153 mU/μg of protein in sapwood and heartwood, respectively, whereas the activity of VP with guaiacol-oxidising properties was very low for all P. abieticola strains, ranging 0–0.248 and 0–0.225 mU/μg of protein in sapwood and heartwood, respectively. The values of released hydroxyphenols in P. abieticola strains ranged 24.915–139.766 and 25.19–84.562 µg of protocatechuic acid/ml in sapwood and heartwood, respectively. The values of released methoxyphenols for the evaluated strains of P. abieticola ranged 7.225–23.789 and 1.953–20.651 µg of vanillic acid/ml in sapwood and heartwood, respectively. Further studies with a higher number of strains of this species as well as an optimisation of conditions for the measurement of ligninolytic activity are needed.

If the inline PDF is not rendering correctly, you can download the PDF file here.

  • Albertó, E.O., Petersen, R.H., Hughes, K.W., Lechner B. 2002. Miscellaneous notes on Pleurotus. Persoonia, 18, 55–69.

  • Agematu, H., Kominato, K., Shibamoto, N., Yoshioka, T. 1993. Transformation of 7-(4-hydroxyphenylacetamido)cephalosporanic acid into a new cephalosporin antibiotic, 7-(1-oxaspiro(2.5)octa-6-oxo-4,7-diene-2-carboxamido)cephalosporanic acid, by laccase. Bioscience Biotechnology and Biochemistry, 57 (8), 1387–1388. DOI: 10.1271/bbb.57.1387

  • Baciocchi, E., Gerini, M.F., Lanzalunga, O., Lapi, A., Piparo, M.G.L., Mancinelli, S. 2001. Isotope-effect profiles in the oxidative N-demethylation of N, N-dimethylanilines catalyzed by lignin peroxidase and a chemical model. European Journal of Organic Chemistry, 2305–2310. DOI: org/10.1002/1099-0690(200106)2001:12˂2305::AID-EJOC2305˃ 3.0.CO;2-E

  • Baldrian, P., Gabriel, J. 2002. Copper and cadmium increase laccase activity in Pleurotus ostreatus. FEMS Microbiology Letters, 206 (1), 69–74. DOI: org/10.1111/j.1574-6968.2002.tb10988.x

  • Baldrian, P. 2005. Fungal laccases occurrence and properties. FEMS Microbiology Review, 30, 215–242. DOI: 10.1111/j.1574–4976.2005.00010.x

  • Baldrian, P., Valášková, V., Merhautová, V., Gabriel, J. 2005. Degradation of lignocellulose by Pleurotus ostreatus in the presence of copper, manganese, lead and zinc. Research in Microbiology, 156, 670–676.

  • Berglung, M., Rӧnnberg, J. 2004. Effectiveness of treatment of Norway spruce stumps with Phlebiopsis gigantea at different rates of coverage for the control of Heterobasidion. Forest Pathology, 34, 233–243.

  • Berglung, M., Rӧnnberg, J., Holmer, L., Stenlid, J. 2005. Comparison of five strains of Phlebiopsis gigantea and two Trichoderma formulations for treatment against natural Heterobasidion spore infections on Norway spruce stumps. Scandinavian Journal of Forest Research, 20 (1), 12–17.

  • Bollag, J.M., Leonowicz, A. 1984. Comparative studies of extracellular fungal laccases. Applied Environmental Microbiology, 48 (4), 849–854.

  • Camarero, S., Bockle, B., Martinez, M.J., Martinez, A.T. 1996. Manganese-Mediated Lignin Degradation by Pleurotus pulmonarius. Applied and Environmental Microbiology, 62 (3), 1070–1072.

  • Camarero, S., Sarkar, S., Ruiz-Dueñas,. FJ., Martinez, M.J., Martinez, A.T. 1999. Description of a versatile peroxidase involved in the natural degradation of lignin that has both manganese peroxidase and lignin peroxidase substrate interaction sites. Journal of Biological Chemistry, 274 (15), 10324–10330.

  • Camassola, M., da Rosa, L.O., Calloni, R., Gaio, T.A., Dillon, A.J.P. 2013. Secretion of laccase and manganese peroxidase by Pleurotus strains cultivate in solid-state using Pinus spp. sawdust. Brazilian Journal of Microbiology, 44 (1), 207–213. DOI: 10.1590/S1517-83822013005000006

  • Cohen, R., Persky, L., Hadar, Y. 2002. Biotechnological applications and potential of wood-degrading mushrooms of the genus Pleurotus. Applied Microbiology and Biotechnology, 58 (5), 582–594. DOI: 10.1007/s00253-002-0930-y

  • Drenkhan, T., Hanso, S., Hanso, M. 2008. Effect of the stump treatment with Phlebiopsis gigantea against Heterobasidion Root Rot in Estonia. Baltic Forestry, 14 (1), 16–25.

  • Elisashvili, V., Kachlishvili, E., Chichua, D., Tsiklauri, N. 2003. Lignocellulolytic enzyme activity during growth and fruiting of the edible and medicinal mushroom Pleurotus ostreatus (Jacq.:Fr.) Kumm. (Agaricomycetideae). International Journal of Medicinal Mushrooms, 5 (2), 193–198.

  • Fåhraeus, G., Tullande, r V., Ljunggren, H. 1958. Production of high laccase yields in cultures of fungi. Physiologia Plantarum, 11, 631–643. DOI: org/10.1111/j.1399-3054.1958.tb08259.x

  • Fåhraeus, G., Reinhammar, B. 1967. Large scale production and purification of laccase from cultures of the fungus Polyporus versicolor and some properties of laccase A. Acta Chemica Scandinavica, 21 (9), 2367–2378.

  • Farnet, A.-M., Tagger, S., Le Petit, J. 1999. Effects of copper and aromatic inducers on the laccasses of the white rot fungus Marasmius quercophilus. Compote Rendus de l’Académie des Sciences – Series III, Sciences de la Vie/Life Sciences, 322 (6), 499–503. DOI: 10.1016/S0764-4469(99)80100-0

  • Garbelotto, M., Gonthier, P. 2013. Biology, epidemiology, and control of Heterobasidion species worldwide. Annual Review of Phytopathology, 51, 39–59. DOI: org/10.1146/annurev-phyto-082712-102225

  • Giardina, P., Palmieri, G., Fontanella, B., Rivieccio, V., Sannia, G. 2000. Manganese peroxidase isoenzymes produced by Pleurotus ostreatus grown on wood sawdust. Archives of Biochemistry and Biophysics, 376, 171–179. DOI: 10.1006/abbi.1999.1691

  • Gierczyk, B., Kujawa, A., Szczepkowski, A. 2015a. The 20th Jubilee Exhibition of Fungi of Białowieża Forest. Study materials on mycobiota of Białowieża Primeval Forest (in Polish with English summary). Przegląd Przyrodniczy, 26, 1, 11–29.

  • Gierczyk, B., Kujawa, A., Szczepkowski, A. Ślusarczyk, T., Kozak, M., Mleczko, P. 2015b. The 21st Exhibition of Fungi of Białowieża Forest. Materials to the knowledge of mycobiota of the Białowieża Primeval Forest (in Polish with English summary). Przegląd Przyrodniczy, 26, 3, 10–50.

  • Gierczyk, B., Ślusarczyk, T., Szczepkowski, A., Kujawa, A. 2017. The 22st Exhibition of Fungi of the Białowieża Forest. Materials to the knowledge of mycobiota of the Białowieża Primeval Forest (in Polish with English summary). Przegląd Przyrodniczy, 28 (1), 59–84.

  • Gierczyk, B., Ślusarczyk, T., Szczepkowski, A., Kujawa, A. 2018. The 23t h Exhibition of Fungi of the Białowieża Forest. Materials to the knowledge of mycobiota of the Białowieża Primeval Forest (in Polish with English summary). Przegląd Przyrodniczy, 29 (2), 9–57.

  • Greig, B.J.W., Gibbs, J.N., Pratt, J.E. 2001. Experiments on the susceptibility of conifers to Heterobasidion annosum in Great Britain. Forest Pathology, 31, 219–228.

  • Gunulf, A., Mc Carthy, R., Rönnberg, J. 2012. Control efficacy of stump treatment and influence of stump height on natural spore infection by Heterobasidion spp. of precommercial thinning stumps of Norway spruce and birch. Silva Fennica, 46 (5), 655–665.

  • Hammel, K.E,. Jensen, K., Mozuch, M., Landucci, L., Tien, M., Pease, E. 1993. Ligninolysis by a purified lignin peroxidase. Journal of Biological Chemistry, 268, 12274–12281.

  • Hatakka, A. 1994. Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiology Reviews, 13, 125–135. DOI: org/10.1111/j.1574-6976.1994. tb00039.x

  • Heinfling, A., Martinez, M.J., Martinez, A.T., Bergbauer, M., Szewczyk, U. 1998a. Purification and characterization of peroxidases from the dyedecolorizing fungus Bjerkandera adusta. FEMS Microbiology Letter, 165 (1), 43–50.

  • Heinfling, A., Martinez, M.J., Martinez, A.T., Bergbauer, M., Szewczyk, U. 1998b. Transformation of industrial dyes by manganese peroxidases from Bjerkandera adusta and Pleurotus eryngii in a manganese-independent reaction. Applied and Environmental Microbiology, 64 (8), 2788–2793.

  • Harkin, J.M., Obst, J.R. 1973. Syringaldazine, an effective reagent for detecting laccase and peroxidase in fungi. Experientia, 29 (4), 381–508. DOI: 10.1007/bf01926734

  • Harvey, P.J., Schoemaker, H.E., Palmer, J.M. 1986. Veratryl alcohol as a mediator and the role of radical cations in lignin biodegradation by Phanerochaete chrysosporium. FEBS Letters, 195, 242–246. DOI: org/10.1016/0014-5793(86)80168-5

  • Harvey, P.J., Palmer, J.M. 1990. Oxidation of phenolic compounds by ligninase. Journal of Biotechnology, 13 (2/3), 169–179. DOI: org/10.1016/0168-1656(90)90102-H

  • Hoegger, P.J., Majcherczyk, A., Dwivedi, R.C., Svobodová, K., Kilaru, S., Kües, U. 2007. Enzymes in wood degradation. In: Wood Production, Wood Technology and Biotechnological Impacts (ed.: U. Kües). Universitätsverlag Gӧttingen, Germany, 389–438.

  • Holdenrieder, O., Engesser, R., Sieber, T.N. 1998. Biological control of Heterobasidion annosum with Phlebiopsis gigantea on Norway spruce in Switzerland. In: Root and Butt Rots of Forest Trees. 9th International Conference on Root and Butt Rots, September 1–7, 1997 (eds.: C. Delatour, J.-J. Guillaumin, B. Lung-Escarmant, B. Marçais). Carcans-Maubuisson, France, 447.

  • Kamitsuji, H., Honda, Y., Watanabe, T., Kuwahara, M. 2004. Production and induction of manganese peroxidase isozymes in a white-rot fungus Pleurotus ostreatus. Applied Microbiology and Biotechnology, 65, 287–294.

  • Kerem, Z., Hadar, Y. 1993. Effect of manganese on lignin degradation by Pleurotus ostreatus during solid-state fermentation. Applied and Environmental Microbiology, 59 (12), 4115–4120.

  • Kerem, Z., Hadar, Y. 1995. Effect of manganese on preferential degradation of lignin by Pleurotus ostreatus during solid-state fermentation. Applied and Environmental Microbiology, 61 (8), 3057–3062.

  • Kodrik, M. 2001. Results of beech stump inoculation with antagonistic fungi. Journal of Forest Science, 47 (11), 505–512.

  • Korhonen, K., Holdenrieder, O. 2005. Recent advances in research on the root rot fungus Heterobasidion annosum s.l. A literature review (in German). Forst und Holz, 60, 206–211.

  • Korhonen, K. et al. 1994. Control of Heterobasidion annosum by stump treatment with “Rotstop”, a new commercial formulation of Phlebiopsis gigantea. In: Proceedings of the 8th International Conference on Root and Butt Rots. Wik, Sweden and Haikko, Finland, August 9–16, 1993. IUFRO Working Party S2.06.01. (eds.: M. Johansson, J. Stenlid). Swedish University of Agricultural Sciences, Uppsala, Sweden, 662–667.

  • Kujawa, A., Gierczyk, B., Kozak, M., Mleczko, P., Ślusarczyk, T. 2017. Diversity of agaricoid, boletoid and hypogeous macrofungi in the Białowieża Forest – project concept and preliminary results. (in Polish with English summary). Fragmenta Floristica et Geobotanica Polonica, 24 (1), 119–131.

  • Leonowicz, A., Grzywnowicz, K. 1981. Quantitative estimation of laccase forms in some white-rot fungi using syringaldazine as a substrate. Enzyme Microbial Technology, 3, 55–58. DOI: org/10.1016/0141-0229(81)90036-3

  • Leonowicz, A., Wojtowicz, B., Trojanowski, J. 1968. Model experiment on the humification of rye roots. I. Phenolic products in the humification process. Polish Journal of Soil Science,1, 129–136.

  • Leonowicz, A., Matuszewka, A., Luterek, J., Ziegenhagen, D., Wojtas-Wasilewska, M. 1999. Biodegradation of lignin by white rot fungi. Fungal Genetics and Biology, 27, 175–185.

  • Li, Y., Liu, Y., Li, T.H. 2014. Flora fungorum sinicorum. Vol. 45. Pleurotoid-lentinoid fungi (in Chinese). Science Press, Beijing.

  • Liu, X.-B., Liu, J.-W., Yang, Z.-L. 2015. A new edible mushroom resource, Pleurotus abieticola, in southwestern China. Mycosystema, 34 (4), 581–588. DOI: 10.13346/j.mycosystema.150051

  • Lundell, T., Wever, R., Floris, R., Harvey, P., Hatakka, A., Brunow, G., Schoemaker, H. 1993. Lignin peroxidase L3 from Phlebia radiata. Pre-steady-state and steady-state studies with veratryl alcohol and a non-phenolic lignin model compound 1-(3,4-dimethoxyphenyl)-2-(2-methoxyphenoxy) propane-1,3-diol. European Journal of Biochemistry, 211, 391–402.

  • Łakomy, P., Werner, A. 2003. Distribution of Heterobasidion annosum intersterility groups in Poland. Forest Pathology, 33 (2), 105–112. DOI: 10.1046/j.1439-0329.2003.00309.x

  • Malarczyk, E. 1984. Substrate−induction of veratric acid O−demethylase in Nocardia sp. Acta Biochimica Polonica, 31 (4), 383−395.

  • Małecka, M. 2019. Choroby infekcyjne. In: Krótkoterminowa prognoza występowania ważniejszych szkodników i chorób infekcyjnych drzew leśnych w Polsce w 2019 r. Instytut Badawczy Leśnictwa (in Polish). Analizy i Raporty, 31, 71–82.

  • Martinez, M.J., Ruiz-Dueñas, F.J., Guillén, F., Martinez, A.T. 1996. Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus eryngii. European Journal of Biochemistry, 237, 424–432. DOI: org/10.1111/j.1432-1033.1996.0424k.x

  • Matuszewska, A. 2005. The influence of mediators on the degradation of model lignin preparations by Trametes versicolor (in Polish). Doctoral dissertation, UMCS Lublin.

  • Mester, T., Field, J.A. 1998. Characterization of a novel manganese peroxidase hybrid isozyme produced by Bjerkandera species strain BOS55 in the absence of manganese. Journal of Biological Chemistry, 273, 15412–15417. DOI: org/10.1074/jbc.273.25.15412

  • Mester T, Field JA. 1998. Characterization of a novel manganese peroxidase-lignin peroxidase hybrid isozyme produced by Bjerkandera species strain BOS55 in the absence of manganese. J Biol Chem 273:15412–15417

  • Nicolotti, G., Gonthier, P., Varese, G.C. 1999. Effectiveness of some biological and chemical treatment against Heterobasidion annosum on Norway spruce stumps. European Journal of Forest Pathology, 29, 339–346.

  • Nicolotti, G., Gonthier, P. 2005. Stump treatment against Heterobasidion with Phlebiopsis gigantea and some chemicals in Picea abies stands in the western Alps. Forest Pathology, 35, 365–374.

  • Petersen, R.H., Hughes, K.W. 1997. A new species of Pleurotus. Mycologia, 89 (1), 173–180.

  • Rishbeth, J. 1951a. Observations on the biology of Fomes annosus, with particular reference to East Anglian pine plantations. II. Spore production, stump infection, and saprophytic activity in stumps. Annals of Botany, 15, 1–21.

  • Rishbeth, J. 1951b. Observation on the biology of Fomes annosus, with particular reference to East Anglian pine plantations. III. Natural and experimental infection of pines, and some factors affecting severity of the disease. Annals of Botany, 15, 221–246.

  • Rishbeth, J. 1957. Some further observation on Fomes annosus Fr. Forestry, 30, 69–89.

  • Rogalski, J., Leonowicz, A. 1992. Phlebia radiata laccase forms induced by veratric acid and xylidine in relation to lignin peroxidase and manganese-dependent peroxidase. Acta Biotechnologica, 12 (3), 213–221. DOI: 10.1002/abio.370120310

  • Rönnberg, J., Cleary, M.R. 2012. Presence of Heterobasidion annosum infections in Norway spruce stumps six years after treatment with Phlebiopsis gigantea. Forest Pathology, 42 (2), 144–149. DOI: org/10.1111/j.1439-0329.2011.00731.x

  • Rönnberg, J., Sidorov, E., Petrylaitė, E. 2006. Efficacy of different concentrations of Rotstop® and Rotstop® S and imperfect coverage of Rotstop® S against Heterobasidion spp. spore infections on Norway spruce stumps. Forest Pathology, 36 (6), 422–433. DOI: org/10.1111/j.1439-0329.2006.00476.x

  • Ruiz-Dueñas, F.J., Camarero, S., Pérez-Boada, M., Martinez, M.J., Martinez, A.T. 2001. A new versatile peroxidase from Pleurotus. Biochemical Society Transactions, 29 (2), 116–122. DOI: 10.1042/BST0290116

  • Sarkar, S., Martinez, A.T., Martinez, M.J. 1997. Biochemical and molecular characterization of a manganese peroxidase isoenzyme from Pleurotus ostreatus. Biochimica et Biophysica Acta, 1339, 23–30. DOI: 10.1016/S0167-4838(96)00201-4

  • Schwarze, F.W.M.R., Engels, J., Mattheck, C. 2000. Fungal strategies of wood decay in trees. Springer-Verlag Berlin, Heidelberg, New York.

  • Schoemaker, H.E., Lundell, T.K., Hatakka, A.I., Piontek, K. 1994. The oxidation of veratryl alcohol, dimeric lignin models and lignin by lignin peroxidase - the redox cycle revisited. FEMS Microbiol Review, 13, 321–332.

  • Sierota, Z. 2001. Choroby lasu (in Polish). Centrum Informacyjne Lasów Państwowych, Warszawa.

  • Stajić, M., Persky, L., Cohen, E., Hadar, Y., Brceski, I., Wasser, S.P., Nevo, E. 2004. Screening of the laccase, manganese peroxidase, and versatile peroxidase activities of the genus Pleurotus in media with some raw plant materials as carbon sources. Applied Biochemistry and Biotechnology, 117 (3), 155–164.

  • Stajić, M., Persky, L., Friesem, D., Hadr, Y., Wasser, S.P., Nevo, E., Vukojević, J. 2006. Effect of different carbon and nitrogen sources on laccase and peroxidases production by selected Pleurotus species. Enzyme and Microbial Technology, 38, 65–73.

  • Stajić, M., Vukojević, J., Knežević, A., Milovanović, I. 2013. Influence of trace elements on ligninolytic enzyme activity of Pleurotus ostratus and P. pulmonarius. Bioresources, 8 (2), 3027–3037. DOI: 10.15376/biores.8.2.3027-3037

  • Stenlid, J., Redfern, D.B. 1998. Spread within the tree and stand. In: Heterobasidion annosum. Biology, ecology, impact and control (eds.: S. Woodward, J. Stenlid, R. Karjalainen, A. Hüttermann). CAB International, Wallingford, UK, 125–141.

  • Sugano, Y., Matsushima, Y., Shoda, M. 2006. Complete decolorization of antraquinone dye Reactive blue 5 by the concerted action of two peroxidases from Thanatephorus cucumeris Dec 1. Applied and Environmental Microbiology, 73 (4), 862871.

  • Szczepkowski, A., Piętka, J. 2008. Results of inoculation of beech (Fagus sylvatica L.) and oak (Quercus sp.) stumps with Pleurotus ostreatus (Jacq.: Fr.) Kumm. Folia Forestalia PolonicaSeries A – Forestry, 49/50, 15–25.

  • Tien, T., Kirk, K. 1988. Lignin peroxidase of Phanerochaete chrysosporium. Methods in Enzymology, 161, 238−249. DOI: 10.1016/0076-6879(88)61025-1

  • Wariishi, H., Gold, M.H. 1989. Lignin peroxidase compound III: formation, inactivation, and conversion to the native enzyme. FEBS Letters, 243, 165–168. DOI: org/10.1016/0014-5793(89)80122-X

  • Wariishi, H., Valli, K., Gold, H.M. 1992. Manganese (II) oxidation by manganese peroxidase from the Basidiomycete Phanerochaete chrysosporium. Journal of Biological Chemistry, 267, 2368523695.

  • Wong, D.W.S. 2009. Structure and action mechanism of ligninolytic enzymes. Applied Biochemistry and Biotechnology, 157, 14−209.

  • Woodward, S., Stenlid, J., Karjalainen, R., Hüttermann, A. 1998. Heterobasidion annosum. Biology, ecology, impact and control. Preface. Cab International, Wallingford, UK.

  • Żółciak, A. 2002. Deciduous stump inoculation with Pleurotus ostreatus as biological method of Armillaria root rot control (in Polish with English summary). Prace Instytutu Badawczego LeśnictwaSeria A, 944, 5–20.

  • Żółciak, A., Korniłłowicz-Kowalska, T.A., Sierota, Z., Iglik, H. 2008. Enzymatic activity of Phlebiopsis gigantea isolates. Acta Mycologica, 43 (1), 41–48.

  • Żółciak, A., Sierota, Z., Małecka, M. 2012. Characterization of some Phlebiopsis gigantea isolates with respect to enzymatic activity and decay of Norway spruce wood. Biocontrol Science and Technology, 22 (7), 777–790. DOI: org/10.1080 /09583157.2012.691156

  • Żółciak, A., Bohacz, J. 2016. Ligninolytic activity of Heterobasidion parviporum isolates in cultivation on Norway spruce wood (in Polish with English summary). Sylwan, 160 (12), 1027−1036.

OPEN ACCESS

Journal + Issues

Search