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Folia Microbiologica

, Volume 51, Issue 6, pp 579–590 | Cite as

Production of lignocellulose-degrading enzymes and changes in soil bacterial communities during the growth ofPleurotus ostreatus in soil with different carbon content

  • J. Šnajdr
  • P. Baldrian
Article

Abstract

The extracellular enzyme activity and changes in soil bacterial community during the growth of the ligninolytic fungusPleurotus ostreatus were determined in nonsterile soil with low and high available carbon content. In soil withP. ostreatus, the activity of ligninolytic enzymes laccase and Mn-peroxidase was several orders of magnitude higher than in soil without the fungus. Addition of lignocellulose to soil increased the activity of cellulolytic fungi and the production of Mn-peroxidase byP. ostreatus. The counts of heterotrophic bacteria were more significantly affected by the presence of lignocellulose than byP. ostreatus. The effects of both substrate addition and time (succession) were more significant factors affecting the soil bacterial community than the presence ofP. ostreatus. Bacterial community structure was affected by fungal colonization in low carbon soil, where a decrease of diversity and changes in substrate utilization profiles were detected.

Keywords

Laccase Activity Ligninolytic Enzyme Nonsterile Soil Ligninolytic Fungus Hemicellulolytic Enzyme 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Abbreviations

ABTS

2,2′-azinobis-3-ethylbenzothiazoline-6-sulfonic acid

CFU

colony forming unit(s)

CTC

circadian temperature cycle

DMAB

3,3-dimethylaminobenzoic acid

EDTA

ethylenediamine tetraacetate

MBTH

3-methyl-2-benzothiazolinone hydrazone

MnP

manganese peroxidase

PAH

oligocyclic (‘polycyclic’) aromatic hydrocarbons

PO

treatment containing nonsterile soil inoculated withP. ostreatus

POS

treatment containing nonsterile soil with straw addition inoculated withP. ostreatus

SO

treatment containing nonsterile soil

SOS

treatment containing nonsterile soil with straw addition

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References

  1. van Aarle I.M., Olsson P.A., Soderstrom B.: Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization.New Phytol. 155, 173–182 (2002).CrossRefGoogle Scholar
  2. Ali T.A., Wainwright A.M.: Growth ofPhanerochaete chrysosporium in soil and its ability to degrade the fungicide benomyl.Biores.Technol. 49, 197–201 (1994).CrossRefGoogle Scholar
  3. Andersson B.E., Welinder L., Olsson P.A., Olsson S., Henrysson T.: Growth of inoculated white-rot fungi and their interactions with the bacterial community in soil contaminated with polycyclic aromatic hydrocarbons, as measured by phospholipid fatty acids.Biores.Technol. 73, 29–36 (2000).CrossRefGoogle Scholar
  4. Andersson B.E., Lundstedt S., Tornberg K., Schnurer Y., Oberg L.G., Mattiasson B.: Incomplete degradation of polycyclic aromatic hydrocarbons in soil inoculated with wood-rotting fungi and their effect on the indigenous soil bacteria.Environ. Toxicol.Chem. 22, 1238–1243 (2003).CrossRefPubMedGoogle Scholar
  5. Baborová P., Móder M., Baldrian P., Cajthamlová K., Cajthaml T.: Purification of a new manganese peroxidase of the white-rot fungusIrpex lacteus and degradation of polycyclic aromatic hydrocarbons by the enzyme.Res.Microbiol. 157, 248–253 (2006).CrossRefPubMedGoogle Scholar
  6. Baldrian P.: Increase of laccase activity during interspecific interactions of white-rot fungi.FEMS Microbiol.Ecol. 50, 245–253 (2004).CrossRefPubMedGoogle Scholar
  7. Baldrian P.: Fungal laccases — occurence and properties.FEMS Microbiol.Rev. 30, 215–242 (2006).CrossRefPubMedGoogle Scholar
  8. Baldrian P., in der Wiesche C., Gabriel J., Nerud F., Zadrazil F.: Influence of cadmium and mercury on activities of ligninolytic enzymes and degradation of polycyclic aromatic hydrocarbons byPleurotus ostreatus in soil.Appl.Environ.Microbiol. 66, 2471–2478 (2000).CrossRefPubMedGoogle Scholar
  9. Baldrian P., Valášková V., Merhautová V., Gabriel J.: Degradation of lignocellulose byPleurotus ostreatus in the presence of copper, manganese, lead and zinc.Res.Microbiol. 156, 670–676 (2005).CrossRefPubMedGoogle Scholar
  10. de Boer W., Folman L.B., Summerbell R.C., Boddy L.: Living in a fungal world: impact of fungi on soil bacterial niche development.FEMS Microbiol.Rev. 29, 795–811 (2005).CrossRefPubMedGoogle Scholar
  11. Bogan B.W., Schoenike B., Lamar R.T., Cullen D.: Manganese peroxidase mRNA and enzyme activity levels during bioremediation of polycyclic aromatic hydrocarbon-contaminated soil withPhanerochaete chrysosporium.Appl.Environ.Microbiol. 62, 2381–2386 (1996a).PubMedGoogle Scholar
  12. Bogan B.W., Schoenike B., Lamar R.T., Cullen D.: Expression oflip genes during growth in soil and oxidation of anthracene byPhanerochaete chrysosporium.Appl.Environ.Microbiol. 62, 3697–3703 (1996b).PubMedGoogle Scholar
  13. Bogan B.W., Lamar R.T., Burgos W.D., Tien M.: Extent of humification of anthracene, fluoranthene, and benzo[a]pyrene byPleurotus ostreatus during growth in PAH-contaminated soils.Lett.Appl.Microbiol. 28, 250–254 (1999).CrossRefGoogle Scholar
  14. Canet R., Birnstingl J.G., Malcolm D.G., Lopez-Real J.M., Beck A.J.: Biodegradation of polycyclic aromatic hydrocarbons (PAHs) by native microflora and combinations of white-rot fungi in a coal-tar contaminated soil.Biores.Technol. 76, 113–117 (2001).CrossRefGoogle Scholar
  15. Criquet S., Tagger S., Vogt G., Iacazio G., Le Petit J.: Laccase activity of forest litter.Soil Biol.Biochem. 31, 1239–1244 (1999).CrossRefGoogle Scholar
  16. Criquet S., Farnet A.M., Tagger S., Le Petit J.: Annual variations of phenol oxidase activities in an evergreen oak litter: influence of certain biotic and abiotic factors.Soil Biol.Biochem. 32, 1505–1513 (2000).CrossRefGoogle Scholar
  17. Criquet S., Tagger S., Vogt G., Le Petit J.: Endoglucanase and β-glycosidase activities in an evergreen oak litter: annual variation and regulating factors.Soil Biol.Biochem. 34, 1111–1120 (2002).CrossRefGoogle Scholar
  18. D’Annibale A., Ricci M., Leonardi V., Quaratino D., Mincione E., Petruccioli M.: Degradation of aromatic hydrocarbons by white-rot fungi in a historically contaminated soil.Biotechnol.Bioeng. 90, 723–731 (2005).CrossRefPubMedGoogle Scholar
  19. Eggen T., Majcherczyk A.: Removal of polycyclic aromatic hydrocarbons (PAH) in contaminated soil by white rot fungusPleurotus ostreatus.Int.Biodeter.Biodegrad. 41, 111–117 (1998).CrossRefGoogle Scholar
  20. Eggen T., Sveum P.: Decontamination of aged creosote polluted soil: the influence of temperature, white rot fungusPleurotus ostreatus, and pretreatment.Int.Biodeter.Biodegrad. 43, 125–133 (1999).CrossRefGoogle Scholar
  21. Eggert C.: Laccase-catalyzed formation of cinnabarinic acid is responsible for antibacterial activity ofPycnoporus cinnabarinus.Microbiol.Res. 152, 315–318 (1997).PubMedGoogle Scholar
  22. Falcon M.A., Rodriguez A., Carnicero A., Regalado V., Perestelo V., Milstein O., De la Fuente G.: Isolation of microorganisms with lignin transformation potential from soil of Tenerife island.Soil Biol.Biochem. 27, 121–126 (1995).CrossRefGoogle Scholar
  23. Fernandez-Sanchez J.M., Rodriguez-Vazquez R., Ruiz-Aguilar G., Alvarez P.J.J.: PCB biodegradation in aged contaminated soil: interactions between exogenousPhanerochaete chrysosporium and indigenous microorganisms.J.Environ.Sci.Health Part A — Toxic/Hazard.Subst.Environ.Eng. 36, 1145–1162 (2001).Google Scholar
  24. Filip Z., Claus H., Dippell G.: Degradation of humic substances by soil microorganisms — a review.Z.Pflnahr.Bodenkd. 161, 605–612 (1998).Google Scholar
  25. Fragoeiro S., Magan N.: Enzymatic activity, osmotic stress and degradation of pesticide mixtures in soil extract liquid broth inoculated withPhanerochaete chrysosporium andTrametes versicolor.Environ.Microbiol. 7, 348–355 (2005).CrossRefPubMedGoogle Scholar
  26. Gramss G.: Activity of oxidative enzymes in fungal mycelia from grassland and forest soils.J.Basic Microbiol. 37, 407–423 (1997).CrossRefGoogle Scholar
  27. Gramss G., Kirsche B., Voigt K.D., Gunther T., Fritsche W.: Conversion rates of five polycyclic aromatic hydrocarbons in liquid cultures of fifty-eight fungi and the concomitant production of oxidative enzymes.Mycol.Res. 103, 1009–1018 (1999a).CrossRefGoogle Scholar
  28. Gramss G., Voigt K.D., Kirsche B.: Degradation of polycyclic aromatic hydrocarbons with three to seven aromatic rings by higher fungi in sterile and unsterile soils.Biodegradation 10, 51–62 (1999b).CrossRefPubMedGoogle Scholar
  29. Gryndler M., Hršelová H., Klír J., Kubát J., Votruba J.: Long-term fertilization affects the abundance of saprotrophic microfungi degrading resistant forms of soil organic matter.Folia Microbiol. 48, 76–82 (2003).CrossRefGoogle Scholar
  30. Harch B.D., Correll R.L., Meech W., Kirkby C.A., Pankhurst C.E.: Using the Gini coefficient with BIOLOG substrate utilization data to provide an alternative quantitative measure for comparing bacterial soil communities.J.Microbiol.Meth. 30, 91–101 (1997).CrossRefGoogle Scholar
  31. Hatakka A.: Biodegradation of lignin, pp. 129–179 in M. Hofrichter, A. Steinbüchel (Eds):Lignin, Humic Substances and Coal. Wiley-VCH, Weinheim 2001.Google Scholar
  32. Hofrichter M.:Review: Lignin conversion by manganese peroxidase (MnP).Enzyme Microb.Technol. 30, 454–466 (2002).CrossRefGoogle Scholar
  33. Kölbel-Boelke J., Tienken B., Nehrkorn A.: Microbial communities in the saturated groundwater environment. 1. Methods of isolation and characterization of heterotrophic bacteria.Microb.Ecol. 16, 17–29 (1988).CrossRefGoogle Scholar
  34. Kotterman M.J.J., Vis E.H., Field J.A.: Successive mineralization and detoxification of benzo[a]pyrene by the white rot fungusBjerkandera sp. strain BOS55 and indigenous microflora.Appl.Environ.Microbiol. 64, 2853–2858 (1998).PubMedGoogle Scholar
  35. Kourtev P.S., Ehrenfeld J.G., Huang W.Z.: Enzyme activities during litter decomposition of two exotic and two native plant species in hardwood forests of New Jersey.Soil Biol.Biochem. 34, 1207–1218 (2002).CrossRefGoogle Scholar
  36. Lang E., Kleeberg I., Zadrazil F.: Competition ofPleurotus sp. andDichomitus squalens with soil microorganisms during lignocellulose decomposition.Biores.Technol. 60, 95–99 (1997a).CrossRefGoogle Scholar
  37. Lang E., Eller G., Zadrazil F.: Lignocellulose decomposition and production of ligninolytic enzymes during interaction of white rot fungi with soil microorganisms.Microb.Ecol. 34, 1–10 (1997b).CrossRefPubMedGoogle Scholar
  38. Lang E., Nerud F., Zadrazil F.: Production of ligninolytic enzymes byPleurotus sp. andDichomitus squalens in soil and lignocellulose substrate as influenced by soil microorganisms.FEMS Microbiol.Lett. 167, 239–244 (1998).CrossRefGoogle Scholar
  39. Lang E., Kleeberg I., Zadrazil F.: Extractable organic carbon and counts of bacteria near the lignocellulose-soil interface during the interaction of soil microbiota and white rot fungi.Biores.Technol. 75, 57–65 (2000).CrossRefGoogle Scholar
  40. Luis P., Kellner H., Martin F., Buscot F.: A molecular method to evaluate basidiomycete laccase gene expression in forest soils.Geoderma 128, 18–27 (2005).CrossRefGoogle Scholar
  41. Martens R., Zadrazil F.: Screening of white-rot fungi for their ability to mincralize polycyclic aromatic hydrocarbons in soil.Folia Microbiol. 43, 97–103 (1998).CrossRefGoogle Scholar
  42. Ngo T.T., Lenhoff H.M.: A sensitive and versatile chromogenic assay for peroxidase and peroxidase-coupled reactions.Anal.Biochem. 105, 389–397 (1980).CrossRefPubMedGoogle Scholar
  43. Niku-Paavola M.L., Raaska L., Itävaara M.: Detection of white-rot fungi by a non-toxic stain.Mycol.Res. 94, 27–31 (1990).CrossRefGoogle Scholar
  44. Rama R., Sigoillot J.C., Chaplain V., Asther M., Jolivalt C., Mougin C.: Inoculation of filamentous fungi in manufactured gas plant site soils and PAH transformation.Polycycl.Arom.Comp. 18, 397–414 (2001).CrossRefGoogle Scholar
  45. Rayner A.D.M., Boddy L.:Decomposition of Wood: Its Biology and Ecology. John Wiley, Chichester (UK) 1998.Google Scholar
  46. Rodriguez A., Perestelo F., Carnicero A., Regalado V., Perez R., De la Fuente G., Falcon M.A.: Degradation of natural lignins and lignocellulosic substrates by soil-inhabiting fungi imperfecti.FEMS Microbiol.Ecol. 21, 213–219 (1996).CrossRefGoogle Scholar
  47. Ruttimann C., Vicuna R., Mozuch M.D., Kirk T.K.: Limited bacterial mineralization of fungal degradation intermediates from synthetic lignin.Appl.Environ.Microbiol. 57, 3652–3655 (1991).PubMedGoogle Scholar
  48. Saparrat M.C.N., Guillén F.: Ligninolytic ability and potential biotechnology applications of the South American fungusPleurotus laciniatocrenatus.Folia Microbiol. 50, 155–160 (2005).CrossRefGoogle Scholar
  49. Steffen K.T., Hatakka A., Hofrichter M.: Degradation of humic acids by the litter-decomposing basidiomyceteCollybia dryophila.Appl.Environ.Microbiol. 68, 3442–3448 (2002).CrossRefPubMedGoogle Scholar
  50. Tornberg K., Baath E., Olsson S.: Fungal growth and effects of different wood decomposing fungi on the indigenous bacterial community of polluted and unpolluted soils.Biol.Fertil.Soils 37, 190–197 (2003).Google Scholar
  51. Tucker B., Radtke C., Kwon S.I., Anderson A.J.: Suppression of bioremediation byPhanerochaete chrysosporium by soil factors.J.Hazard.Mater. 41, 251–265 (1995).CrossRefGoogle Scholar
  52. Tuomela M., Lyytikaeinen M., Oivanen P., Hatakka A.: Mineralization and conversion of pentachlorophenol (PCP) in soil inoculated with the white-rot fungusTrametes versicolor.Soil Biol.Biochem. 31, 65–74 (1999).CrossRefGoogle Scholar
  53. Wells J.M., Harris M.J., Boddy L.: Encounter with new resources causes polarized growth of the cord-forming basidiomycetePhanerochaete velutina on soil.Microb.Ecol. 36, 372–382 (1998).CrossRefPubMedGoogle Scholar
  54. in der Wiesche C., Martens R., Zadrazil F.: Two-step degradation of pyrene by white-rot fungi and soil microorganisms.Appl. Microbiol.Biotechnol. 46, 653–659 (1996).CrossRefPubMedGoogle Scholar

Copyright information

© Institute of Microbiology, Academy of Sciences of the Czech Republic 2006

Authors and Affiliations

  1. 1.Laboratory of Biochemistry of the Wood-Rotting Fungi, Institute of MicrobiologyAcademy of Sciences of the Czech RepublicPragueCzechia

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