Skip to main content
SpringerLink
Log in

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

  • Published:
Folia Microbiologica Aims and scope Submit manuscript

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.

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

Similar content being viewed by others

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

References

  • 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).

    Article  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • Baldrian P.: Increase of laccase activity during interspecific interactions of white-rot fungi.FEMS Microbiol.Ecol. 50, 245–253 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Baldrian P.: Fungal laccases — occurence and properties.FEMS Microbiol.Rev. 30, 215–242 (2006).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    CAS  PubMed  Google Scholar 

  • 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).

    CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Criquet S., Tagger S., Vogt G., Iacazio G., Le Petit J.: Laccase activity of forest litter.Soil Biol.Biochem. 31, 1239–1244 (1999).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Eggert C.: Laccase-catalyzed formation of cinnabarinic acid is responsible for antibacterial activity ofPycnoporus cinnabarinus.Microbiol.Res. 152, 315–318 (1997).

    CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    CAS  Google Scholar 

  • Filip Z., Claus H., Dippell G.: Degradation of humic substances by soil microorganisms — a review.Z.Pflnahr.Bodenkd. 161, 605–612 (1998).

    CAS  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • Gramss G.: Activity of oxidative enzymes in fungal mycelia from grassland and forest soils.J.Basic Microbiol. 37, 407–423 (1997).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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 

  • Hofrichter M.:Review: Lignin conversion by manganese peroxidase (MnP).Enzyme Microb.Technol. 30, 454–466 (2002).

    Article  CAS  Google Scholar 

  • 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).

    Article  Google Scholar 

  • 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).

    CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Lang E., Kleeberg I., Zadrazil F.: Competition ofPleurotus sp. andDichomitus squalens with soil microorganisms during lignocellulose decomposition.Biores.Technol. 60, 95–99 (1997a).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Ngo T.T., Lenhoff H.M.: A sensitive and versatile chromogenic assay for peroxidase and peroxidase-coupled reactions.Anal.Biochem. 105, 389–397 (1980).

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • Rayner A.D.M., Boddy L.:Decomposition of Wood: Its Biology and Ecology. John Wiley, Chichester (UK) 1998.

    Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    CAS  PubMed  Google Scholar 

  • Saparrat M.C.N., Guillén F.: Ligninolytic ability and potential biotechnology applications of the South American fungusPleurotus laciniatocrenatus.Folia Microbiol. 50, 155–160 (2005).

    Article  CAS  Google Scholar 

  • Steffen K.T., Hatakka A., Hofrichter M.: Degradation of humic acids by the litter-decomposing basidiomyceteCollybia dryophila.Appl.Environ.Microbiol. 68, 3442–3448 (2002).

    Article  CAS  PubMed  Google Scholar 

  • 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).

    CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  CAS  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

  • 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).

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Biochemistry of the Wood-Rotting Fungi, Institute of Microbiology, Academy of Sciences of the Czech Republic, 142 20, Prague, Czechia

    J. Šnajdr & P. Baldrian

Authors
  1. J. Šnajdr
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. P. Baldrian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to P. Baldrian.

Additional information

This study was supported by theCzech Science Foundation (204/02/P100 and 526/05/0168) and by theInstitutional Research Concept no. AV0Z 5020 0510 of theInstitute of Microbiology, Acad. Sci. Czech Rep.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Šnajdr, J., Baldrian, P. Production of lignocellulose-degrading enzymes and changes in soil bacterial communities during the growth ofPleurotus ostreatus in soil with different carbon content. Folia Microbiol 51, 579–590 (2006). https://doi.org/10.1007/BF02931623

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02931623

Keywords

Search

Navigation