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Patchiness and Spatial Distribution of Laccase Genes of Ectomycorrhizal, Saprotrophic, and Unknown Basidiomycetes in the Upper Horizons of a Mixed Forest Cambisol

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Abstract

Decomposition of plant litter by the soil microbial community is an important process of controlling nutrient cycling and soil humus formation. Fungal laccases are key players in litter-associated polyphenol degradation, but little is known about the diversity and spatial distribution of fungal species with laccase genes in soils. Diversity of basidiomycete laccase genes was assessed in a cambisolic forest soil, and the spatial distribution of the sequences was mapped in a 100-m2 plot by using polymerase chain reaction (PCR) on soil DNA extracts. Diversity of laccase sequences was higher in the organic horizon and decreased with the depth. A total of 167 different sequences sharing 44–96% oligonucleotide similarity was found in 13 soil cores harvested in the 100-m2 plot. Dissimilarity in laccase sequence content was 67% between adjacent cores; 45.5%, 35.5% and 19% of laccase sequences were attributed to ectomycorrhizal, unknown and saprotrophic basidiomycetes, respectively. Most dominant sequences were attributed to the extramatrical hyphae of known ectomycorrhizal taxa (e.g., Russulaceae) and restricted to small patches (<0.77 m2) in a specific soil horizon. Soil fungi with laccase genes occupied different niches and showed strikingly variable distribution patterns. The distribution of laccase sequences, and corresponding fungi, likely reflected a part of the oxidative potential in soils.

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References

  1. SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res 25 3389–3402 Occurrence Handle9254694 Occurrence Handle10.1093/nar/25.17.3389 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D

    Article  PubMed  CAS  Google Scholar 

  2. IC Anderson JWG Cairney (2004) ArticleTitleDiversity and ecology of soil fungal communities: increased understanding through the application of molecular techniques Environ Microbiol 6 769–779 Occurrence Handle15250879 Occurrence Handle10.1111/j.1462-2920.2004.00675.x Occurrence Handle1:CAS:528:DC%2BD2cXntVKisLY%3D

    Article  PubMed  CAS  Google Scholar 

  3. IC Anderson CD Campbell JI Prosser (2003) ArticleTitleDiversity of fungi in organic soils under a moorland—Scots pine (Pinus sylvestris L.) gradient Environ Microbiol 5 1121–1132 Occurrence Handle14641592

    PubMed  Google Scholar 

  4. EW Beals (1984) ArticleTitleBray–Curtis ordination: an effective strategy for analysis of multivariate ecological data Adv Ecol Res 14 1–55

    Google Scholar 

  5. GD Bending DJ Read (1997) ArticleTitleLignin and soluble phenolic degradation by ectomycorrhizal and ericoid mycorrhizal fungi Mycol Res 101 1348–1354 Occurrence Handle10.1017/S0953756297004140 Occurrence Handle1:CAS:528:DyaK1cXjtlGruw%3D%3D

    Article  CAS  Google Scholar 

  6. RM Burke JWG Cairney (2002) ArticleTitleLaccases and other polyphenoloxidases in ecto- and ericoid mycorrhizal fungi Mycorrhiza 12 105–116 Occurrence Handle12072980 Occurrence Handle1:CAS:528:DC%2BD38XntF2jtrs%3D Occurrence Handle10.1007/s00572-002-0162-0

    Article  PubMed  CAS  Google Scholar 

  7. RG Burns (1982) ArticleTitleEnzymes activity in soil: location and a possible role in microbial ecology Soil Biol Biochem 14 423–427 Occurrence Handle10.1016/0038-0717(82)90099-2 Occurrence Handle1:CAS:528:DyaL28XoslGgsA%3D%3D

    Article  CAS  Google Scholar 

  8. TD Bruns (1995) ArticleTitleThoughts on the processes that maintain local species diversity of ectomycorrhizal fungi Plant Soil 170 63–73 Occurrence Handle10.1007/BF02183055 Occurrence Handle1:CAS:528:DyaK2MXlt1Kgtbg%3D

    Article  CAS  Google Scholar 

  9. DM Chen BA Bastias AFS Taylor JWG Cairney (2003) ArticleTitleIdentification of laccase-like genes in ectomycorrhizal basidiomycetes and transcriptional regulation by nitrogen in Piloderma byssinum New Phytol 157 547–554 Occurrence Handle10.1046/j.1469-8137.2003.00687.x Occurrence Handle1:CAS:528:DC%2BD3sXisF2gu7Y%3D

    Article  CAS  Google Scholar 

  10. F Corpet (1988) ArticleTitleMultiple sequence alignment with hierarchical clustering Nucleic Acids Res 16 10881–10890 Occurrence Handle2849754 Occurrence Handle1:CAS:528:DyaL1MXjsVOqtA%3D%3D

    PubMed  CAS  Google Scholar 

  11. S Criquet AM Farnet S Tagger J Petit ParticleLe (2000) ArticleTitleAnnual variations of phenoloxidase activities in an evergreen oak litter: influence of certain biotic and abiotic factors Soil Biol Biochem 32 1505–1513 Occurrence Handle10.1016/S0038-0717(00)00027-4 Occurrence Handle1:CAS:528:DC%2BD3cXntFSmu70%3D

    Article  CAS  Google Scholar 

  12. S Daina M Orlandi G Bestetti C Wiik G Elegir (2002) ArticleTitleDegradation of beta-5 lignin model dimers by Ceriporiopsis subvermispora Enzyme Microb Technol 30 499–505 Occurrence Handle10.1016/S0141-0229(01)00524-5 Occurrence Handle1:CAS:528:DC%2BD38Xis1Oqsro%3D

    Article  CAS  Google Scholar 

  13. IA Dickie B Xu RT Koide (2002) ArticleTitleVertical niche differentiation of ectomycorrhizal hyphae in soil as shown by T-RFLP analysis New Phytol 156 527–535 Occurrence Handle10.1046/j.1469-8137.2002.00535.x Occurrence Handle1:CAS:528:DC%2BD38Xpslemt7g%3D

    Article  CAS  Google Scholar 

  14. O Dilly S Bartsch P Rosenbrock F Buscot JC Munch (2001) ArticleTitleShifts in physiological capabilities of the microbiota during the decomposition of leaf litter in a black alder (Alnus glutinosa (Gaertn.) L.) forest Soil Biol Biochem 33 921–930 Occurrence Handle1:CAS:528:DC%2BD3MXksVOrtbY%3D

    CAS  Google Scholar 

  15. C Eggert U Temp KEL Eriksson (1996) ArticleTitleThe ligninolytic system of the white rot fungus Pycnoporus cinnabarinus: purification and characterization of the laccase Appl Environ Microbiol 62 1151–1158 Occurrence Handle8919775 Occurrence Handle1:CAS:528:DyaK28XitFeksL0%3D

    PubMed  CAS  Google Scholar 

  16. C Emmerling M Schloter A Hartmann E Kandeler (2002) ArticleTitleFunctional diversity of soil organisms—a review of recent research activities in Germany J Plant Nutr Soil Sci 165 408–420 Occurrence Handle1:CAS:528:DC%2BD38XmsVKgtb0%3D

    CAS  Google Scholar 

  17. InstitutionalAuthorNameFAO-UNESCO (1990) Soil Map of the World, Revised Legend. World Soil Resources Report 60 FAO Rome

    Google Scholar 

  18. RA Farley AH Fitter (1999) ArticleTitleTemporal and spatial variation in soil resources in a deciduous woodland J Ecol 87 688–696

    Google Scholar 

  19. G Gramss T Guenther W Fritsche (1998) ArticleTitleSpot tests for oxidative enzymes in ectomycorrhizal, wood-, and litter decaying fungi Mycol Res 102 67–72 Occurrence Handle10.1017/S095375629700436X Occurrence Handle1:CAS:528:DyaK1cXhtlGis7Y%3D

    Article  CAS  Google Scholar 

  20. A Guidot JC Debaud A Effosse R Marmeisse (2004) ArticleTitleBelow-ground distribution and persistence of an ectomycorrhizal fungus New Phytol 161 539–547 Occurrence Handle10.1046/j.1469-8137.2003.00945.x Occurrence Handle1:CAS:528:DC%2BD2cXhsVymu70%3D

    Article  CAS  Google Scholar 

  21. DS Hibbett LB Gilbert MJ Donoghue (2000) ArticleTitleEvolutionary instability of ectomycorrhizal symbioses in basidiomycetes Nature 407 506–508 Occurrence Handle11029000 Occurrence Handle10.1038/35035065 Occurrence Handle1:STN:280:DC%2BD3cvnslKgsg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  22. P Högberg AH Plamboeck AFS Taylor PM Fransson (1999) ArticleTitleNatural C13 abundance reveals trophic status of fungi and host-origin of carbon in mycorrhizal fungi in mixed forests Proc Natl Acad Sci USA 96 8534–8539 Occurrence Handle10411910

    PubMed  Google Scholar 

  23. TR Horton TD Bruns (2001) ArticleTitleThe molecular revolution in ectomycorrhizal ecology: peeking into the black box Mol Ecol 10 1855–1871 Occurrence Handle11555231 Occurrence Handle10.1046/j.0962-1083.2001.01333.x Occurrence Handle1:CAS:528:DC%2BD3MXmslyhtr8%3D

    Article  PubMed  CAS  Google Scholar 

  24. A Iakovlev J Stenlid (2000) ArticleTitleSpatiotemporal patterns of laccase activity in interacting mycelia of wood-decaying basidiomycete fungi Microb Ecol 39 236–245 Occurrence Handle12035100 Occurrence Handle1:CAS:528:DC%2BD3cXlsFWjsrw%3D

    PubMed  CAS  Google Scholar 

  25. A Jumpponen (2003) ArticleTitleSoil fungal community assembly in a primary successional glacier forefront ecosystem as inferred from rDNA sequence analyses New Phytol 158 569–578 Occurrence Handle10.1046/j.1469-8137.2003.00767.x

    Article  Google Scholar 

  26. K Kaiser K Eusterhues C Rumpel G Guggenberger I Kögel-Knabner (2002) ArticleTitleStabilization of organic matter by soil minerals—investigations of density and particle-size fractions from two acid forest soils J Plant Nutr Soil Sci 165 451–459 Occurrence Handle10.1002/1522-2624(200208)165:4<451::AID-JPLN451>3.0.CO;2-B Occurrence Handle1:CAS:528:DC%2BD38XmsVKgtbY%3D

    Article  CAS  Google Scholar 

  27. M Kimura (1980) ArticleTitleA simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences J Mol Evol 16 111–120 Occurrence Handle7463489 Occurrence Handle10.1007/BF01731581 Occurrence Handle1:CAS:528:DyaL3MXmtFSktg%3D%3D

    Article  PubMed  CAS  Google Scholar 

  28. R Landeweert P Leeflang TW Kuyper E Hoffland A Rosling K Wernars E Smit (2003) ArticleTitleMolecular identification of ectomycorrhizal mycelium in soil Appl Environ Microbiol 69 327–333 Occurrence Handle12514012 Occurrence Handle10.1128/AEM.69.1.327-333.2003 Occurrence Handle1:CAS:528:DC%2BD3sXkvValsA%3D%3D

    Article  PubMed  CAS  Google Scholar 

  29. EA Lilleskov TD Bruns TR Horton DL Taylor P Grogan (2004) ArticleTitleDetection of forest stand-level spatial structure in ectomycorrhizal fungal communities FEMS Microbiol Ecol 49 319–332 Occurrence Handle1:CAS:528:DC%2BD2cXlsl2hsrY%3D Occurrence Handle19712424

    CAS  PubMed  Google Scholar 

  30. BD Lindahl AFS Taylor (2004) ArticleTitleOccurrence of N-acetylhexosaminidase-encoding genes in ectomycorrhizal basidiomycetes New Phytol 164 193–199 Occurrence Handle10.1111/j.1469-8137.2004.01147.x Occurrence Handle1:CAS:528:DC%2BD2cXovF2rsbc%3D

    Article  CAS  Google Scholar 

  31. Luis, P, Kellner, H, Martin, F, Buscot, F (2005) A molecular method to evaluate basidiomycete laccase gene expression in forest soils. Geoderma 128: 18–27

    Article  CAS  Google Scholar 

  32. P Luis G Walther H Kellner F Martin F Buscot (2004) ArticleTitleDiversity of laccase genes from basidiomycetes in a forest soil Soil Biol Biochem 36 1025–1036 Occurrence Handle10.1016/j.soilbio.2004.02.017 Occurrence Handle1:CAS:528:DC%2BD2cXltVKiurk%3D

    Article  CAS  Google Scholar 

  33. JI Lyons SY Newell A Buchan MA Moran (2003) ArticleTitleDiversity of ascomycete laccase gene sequences in a southeastern US salt marsh Microb Ecol 45 270–281 Occurrence Handle12632211 Occurrence Handle10.1007/s00248-002-1055-7 Occurrence Handle1:CAS:528:DC%2BD3sXkvFGlsL4%3D

    Article  PubMed  CAS  Google Scholar 

  34. M Mansur T Suárez JB Fernández-Larrea MA Brizuela AE González (1997) ArticleTitleIdentification of a laccase gene family in the new lignin-degrading basidiomycete CECT 20197 Appl Environ Microbiol 63 2637–2646 Occurrence Handle9212414 Occurrence Handle1:CAS:528:DyaK2sXktlert7s%3D

    PubMed  CAS  Google Scholar 

  35. N Mantel RS Valand (1970) ArticleTitleA technique of nonparametric multivariate analysis Biometrics 26 547–558 Occurrence Handle5480664 Occurrence Handle1:STN:280:DyaE3M%2FjsFGmtQ%3D%3D

    PubMed  CAS  Google Scholar 

  36. F Martin (2001) ArticleTitleFrontiers in molecular mycorrhizal research—genes, loci, dots and spins New Phytol 150 499–505 Occurrence Handle10.1046/j.1469-8137.2001.00144.x

    Article  Google Scholar 

  37. D Martinez LF Larrondo N Putnam MDS Gelpke K Huang J Chapman KG Helfenbein P Ramaiya JC Detter F Larimer PM Coutinho B Henrissat R Berka D Cullen D Rokhsar (2004) ArticleTitleGenome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78 Nat Biotechnol 22 695–700 Occurrence Handle15122302 Occurrence Handle1:CAS:528:DC%2BD2cXksV2gtro%3D

    PubMed  CAS  Google Scholar 

  38. E Matsumura T Shin S Murao E Yamamoto T Kawano (1987) ArticleTitleNew enzymatic colorimetric reactions of benzoic acid derivatives with ABTS 2,2′-azinobis-3-ethylbenzthiazoline-6-sulfonic acid diammonium salt in the presence of laccase Agric Biol Chem 51 2743–2750 Occurrence Handle1:CAS:528:DyaL1cXjsVansQ%3D%3D

    CAS  Google Scholar 

  39. B McCune JB Grace DL Urban (2002) Analysis of Ecological Communities MjM Software Gleneden Beach, OR

    Google Scholar 

  40. B McCune MJ Mefford (1999) PC-Ord. Multivariate Analysis of Ecological Data, Version 4 MjM Software Design Gleneden Beach, OR

    Google Scholar 

  41. SR Pointing AL Pelling GJD Smith KD Hyde CA Reddy (2005) ArticleTitleScreening of basidiomycetes and xylariaceous fungi for lignin peroxidase and laccase gene-specific sequences Mycol Res 109 115–124 Occurrence Handle15736869 Occurrence Handle10.1017/S0953756204001376 Occurrence Handle1:CAS:528:DC%2BD2MXhtlersrk%3D

    Article  PubMed  CAS  Google Scholar 

  42. C Pyles MM Brown (1999) ArticleTitleHeterogeneity of wood decay classes within hardwood logs For Ecol Manag 114 253–259

    Google Scholar 

  43. WX Schulze G Gleixner K Kaiser G Guggenberger M Mann ED Schulze (2005) ArticleTitleA proteomic fingerprint of dissolved organic carbon and of soil particles Oecologia 142 335–343 Occurrence Handle15449171 Occurrence Handle10.1007/s00442-004-1698-9

    Article  PubMed  Google Scholar 

  44. CE Shannon (1948) ArticleTitleA mathematical theory of communication Bell Syst Tech J 27 379–423

    Google Scholar 

  45. RL Sinsabaugh MM Carreiro S Alvarez (2002) Enzymes and microbial dynamics of litter decomposition RG Burns RP Dick (Eds) Enzymes in the Environment, Activity, Ecology, and Applications Marcel Dekker New York, Basel 249–265

    Google Scholar 

  46. Swofford, DL (1998) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4

  47. AFS Taylor PM Fransson P Högberg MN Högberg AH Plamboeck (2003) ArticleTitleSpecies level patterns in 13C and 15N abundance of ectomycorrhizal and saprotrophic fungal sporocarps New Phytol 159 757–774 Occurrence Handle10.1046/j.1469-8137.2003.00838.x Occurrence Handle1:CAS:528:DC%2BD3sXns1Sgsrg%3D

    Article  CAS  Google Scholar 

  48. L Tedersoo U Kõljalg N Hallenberg KH Larsson (2003) ArticleTitleFine scale distribution of ectomycorrhizal fungi and roots across substrate layers including coarse woody debris in a mixed forest New Phytol 159 153–165 Occurrence Handle10.1046/j.1469-8137.2003.00792.x Occurrence Handle1:CAS:528:DC%2BD3sXlslalt7s%3D

    Article  CAS  Google Scholar 

  49. G Thorn (1997) The fungi in soil JD Elsaß Particlevan JT Trevors EMH Wellington (Eds) Modern Soil Microbiology Marcel Dekker New York 63–128

    Google Scholar 

  50. T Vares M Kalsi A Hatakka (1995) ArticleTitleLignin peroxidases, manganese peroxidases, and other ligninolytic enzymes produced by Phlebia radiata during solid-state fermentation of wheat straw Appl Environ Microbiol 61 3315–3520

    Google Scholar 

  51. JA Wahleithner F Xu KM Brown SH Brown EJ Golightly T Halkier S Kauppinen A Pederson P Schneider (1996) ArticleTitleThe identification and characterization of four laccases from the plant pathogenic fungus Rhizoctonia solani Curr Genet 29 395–403 Occurrence Handle8598061 Occurrence Handle1:CAS:528:DyaK28XitlCnt74%3D

    PubMed  CAS  Google Scholar 

  52. B Wu K Nara T Hogetsu (1999) ArticleTitleCompetition between ectomycorrhizal fungi colonizing Pinus densiflora Mycorrhiza 9 151–159 Occurrence Handle10.1007/s005720050300

    Article  Google Scholar 

  53. AG Zavarzina AA Leontievsky LA Golovleva SY Trofimov (2004) ArticleTitleBiotransformation of soil humic acids by blue laccase of Panus tigrinus 8/18: an in vitro study Soil Biol Biochem 36 359–369 Occurrence Handle10.1016/j.soilbio.2003.10.010 Occurrence Handle1:CAS:528:DC%2BD2cXmvFGqsA%3D%3D

    Article  CAS  Google Scholar 

  54. Z Zhou T Hogetsu (2002) ArticleTitleSubterranean community structure of ectomycorrhizal fungi under Suillus grevillei sporocarps in a Larix kaempferi forest New Phytol 154 529–539 Occurrence Handle10.1046/j.1469-8137.2002.00395.x

    Article  Google Scholar 

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Acknowledgments

This work was financially supported by the Deutsche Forschungsgemeinschaft in the frame of the program “Soils as source and sink of CO2” (SPP1090 grant number Bu 941/2-2). We are indebted to Uwe Hell and Dr. Kalbitz [Institute of Ecosystem Research (BITÖK), University of Bayreuth, Germany] for their help during the soil sampling. We would like to thank Christine Delaruelle and Dr. Annegret Kolher (INRA-Nancy, France) for their help with the laccase gene sequencing.

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  1. Patricia Luis

    Present address: Institute of Biology I, Department of Plant Physiology, University of Leipzig, Johannisallee 21, D-04103, Leipzig, Germany

Authors and Affiliations

  1. Institute of Biology I, Department of Terrestrial Ecology, University of Leipzig, Johannisallee 21, D-04103, Leipzig, Germany

    Patricia Luis, Harald Kellner, Bettina Zimdars & François Buscot

  2. UMR INRA/UHP 1136 “Interactions Arbres/Micro-organismes”, Centre INRA de Nancy, F-54280, Champenoux, France

    Patricia Luis & Francis Martin

  3. UFZ-Umweltforschungszentrum Leipzig-Halle, Soil Research Section, Theodor-Lieser-Str. 4, D-06120, Halle, Germany

    Uwe Langer

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Correspondence to Patricia Luis.

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Luis, P., Kellner, H., Zimdars, B. et al. Patchiness and Spatial Distribution of Laccase Genes of Ectomycorrhizal, Saprotrophic, and Unknown Basidiomycetes in the Upper Horizons of a Mixed Forest Cambisol. Microb Ecol 50, 570–579 (2005). https://doi.org/10.1007/s00248-005-5047-2

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