1887

Abstract

In this paper, we report on the diversity of the mycotrophic fungus (teleomorph Ascomycota, Dikarya) revealed by a taxon-specific metagenomic approach. We designed a set of genus-specific internal transcribed spacer (ITS)1 and ITS2 rRNA primers and constructed a clone library containing 411 molecular operational taxonomic units (MOTUs). The overall species composition in the soil of the two distinct ecosystems in the Danube floodplain consisted of 15 known species and two potentially novel taxa. The latter taxa accounted for only 1.5 % of all MOTUs, suggesting that almost no hidden or uncultivable species are present at least in these temperate forest soils. The species were unevenly distributed in vertical soil profiles although no universal factors controlling the distribution of all of them (chemical soil properties, vegetation type and affinity to rhizosphere) were revealed. experiments simulating infrageneric interactions between the pairs of species that were detected in the same soil horizon showed a broad spectrum of reactions from very strong competition over neutral coexistence to the pronounced synergism. Our data suggest that only a relatively small portion of species is adapted to soil as a habitat and that the interaction between these species should be considered in a screening for as an agent(s) of biological control of pests.

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2012-01-01
2019-12-14
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References

  1. Atanasova L. , Jaklitsch W. M. , Komoń-Zelazowska M. , Kubicek C. P. , Druzhinina I. S. . ( 2010; ). Clonal species Trichoderma parareesei sp. nov. likely resembles the ancestor of the cellulase producer Hypocrea jecorina/T. reesei . . Appl Environ Microbiol 76:, 7259–7267. [CrossRef] [PubMed]
    [Google Scholar]
  2. Batjes N. H. . ( 1996; ). Total carbon and nitrogen in the soils of the world. . Eur J Soil Sci 47:, 151–163. [CrossRef]
    [Google Scholar]
  3. Betina V. , Farkas V. . ( 1998; ). Sporulation and light-induced development in Trichoderma . . In Trichoderma & Gliocladium, vol. 1, pp. 75–94. Edited by Harman G. E. , Kubicek C. P. . . London:: Taylor & Francis;.
    [Google Scholar]
  4. Buée M. , Reich M. , Murat C. , Morin E. , Nilsson R. H. , Uroz S. , Martin F. . ( 2009; ). 454 Pyrosequencing analyses of forest soils reveal an unexpectedly high fungal diversity. . New Phytol 184:, 449–456. [CrossRef] [PubMed]
    [Google Scholar]
  5. Burnett J. . ( 2003; ). Fungal Populations and Species. Oxford:: University Press;.
    [Google Scholar]
  6. Chaverri P. , Castlebury L. A. , Samuels G. J. , Geiser D. M. . ( 2003; ). Multilocus phylogenetic structure within the Trichoderma harzianum/Hypocrea lixii complex. . Mol Phylogenet Evol 27:, 302–313. [CrossRef] [PubMed]
    [Google Scholar]
  7. Colwell, R. K. (2005). EstimateS: statistical estimation of species richness and shared species from samples (version 7.5). User's guide and application, http://viceroy.eeb.uconn.edu/estimates
  8. Druzhinina I. S. , Kopchinskiy A. G. , Komoń M. , Bissett J. , Szakacs G. , Kubicek C. P. . ( 2005; ). An oligonucleotide barcode for species identification in Trichoderma and Hypocrea . . Fungal Genet Biol 42:, 813–828. [CrossRef] [PubMed]
    [Google Scholar]
  9. Druzhinina I. S. , Kopchinskiy A. G. , Kubicek C. P. . ( 2006; ). The first 100 Trichoderma species characterized by molecular data. . Mycoscience 47:, 55–64. [CrossRef]
    [Google Scholar]
  10. Druzhinina I. S. , Komoń-Zelazowska M. , Kredics L. , Hatvani L. , Antal Z. , Belayneh T. , Kubicek C. P. . ( 2008; ). Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable of causing invasive mycoses of humans. . Microbiology 154:, 3447–3459. [CrossRef] [PubMed]
    [Google Scholar]
  11. Druzhinina I. S. , Komoń-Zelazowska M. , Atanasova L. , Seidl V. , Kubicek C. P. . ( 2010a; ). Evolution and ecophysiology of the industrial producer Hypocrea jecorina (Anamorph Trichoderma reesei) and a new sympatric agamospecies related to it. . PLoS ONE 5:, e9191. [CrossRef] [PubMed]
    [Google Scholar]
  12. Druzhinina I. S. , Kubicek C. P. , Komoń-Zelazowska M. , Mulaw T. B. , Bissett J. . ( 2010b; ). The Trichoderma harzianum demon: complex speciation history resulting in coexistence of hypothetical biological species, recent agamospecies and numerous relict lineages. . BMC Evol Biol 10:, 94. [CrossRef] [PubMed]
    [Google Scholar]
  13. Druzhinina I. S. , Seidl-Seiboth V. , Herrera-Estrella A. , Horwitz B. A. , Kenerley C. M. , Monte E. , Mukherjee P. K. , Zeilinger S. , Grigoriev I. V. , Kubicek C. P. . ( 2011; ). Trichoderma: the genomics of opportunistic success. . Nat Rev Microbiol 9:, 749–759. [CrossRef] [PubMed]
    [Google Scholar]
  14. FAO ( 1998; ). World Reference Base for Soil Resources. Rome:: Food and Agriculture Organization of the United Nations;.
    [Google Scholar]
  15. Friedl M. A. , Kubicek C. P. , Druzhinina I. S. . ( 2008; ). Carbon source dependence and photostimulation of conidiation in Hypocrea atroviridis . . Appl Environ Microbiol 74:, 245–250. [CrossRef] [PubMed]
    [Google Scholar]
  16. Gazis R. , Rehner S. , Chaverri P. . ( 2011; ). Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. . Mol Ecol 20:, 3001–3013. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hagn A. , Wallisch S. , Radl V. , Charles Munch J. , Schloter M. . ( 2007; ). A new cultivation independent approach to detect and monitor common Trichoderma species in soils. . J Microbiol Methods 69:, 86–92. [CrossRef] [PubMed]
    [Google Scholar]
  18. Harman G. E. , Howell C. R. , Viterbo A. , Chet I. , Lorito M. . ( 2004; ). Trichoderma species – opportunistic, avirulent plant symbionts. . Nature Rev Microbiol 2:, 43–56. [CrossRef] [PubMed]
    [Google Scholar]
  19. Hawksworth D. L. . ( 1991; ). The fungal dimension of biodiversity: magnitude, significance, and conservation. . Mycol Res 95:, 641–655. [CrossRef]
    [Google Scholar]
  20. Hoyos-Carvajal L. , Orduz S. , Bissett J. . ( 2009; ). Genetic and metabolic biodiversity of Trichoderma from Colombia and adjacent neotropic regions. . Fungal Genet Biol 46:, 615–631. [CrossRef] [PubMed]
    [Google Scholar]
  21. Jaklitsch W. M. . ( 2009; ). European species of Hypocrea Part I. The green-spored species. . Stud Mycol 63:, 1–91. [CrossRef] [PubMed]
    [Google Scholar]
  22. Jaklitsch W. M. . ( 2011; ). European species of Hypocrea. Part II: species with hyaline ascospores. . Fungal Divers 48:, 1–250.[PubMed] [CrossRef]
    [Google Scholar]
  23. Jaklitsch W. M. , Komon M. , Kubicek C. P. , Druzhinina I. S. . ( 2005; ). Hypocrea voglmayrii sp. nov. from the Austrian Alps represents a new phylogenetic clade in Hypocrea/Trichoderma . . Mycologia 97:, 1365–1378. [CrossRef] [PubMed]
    [Google Scholar]
  24. Jaklitsch W. M. , Komon M. , Kubicek C. P. , Druzhinina I. S. . ( 2006a; ). Hypocrea crystalligena sp. nov., a common European species with a white-spored Trichoderma anamorph. . Mycologia 98:, 499–513. [CrossRef] [PubMed]
    [Google Scholar]
  25. Jaklitsch W. M. , Samuels G. J. , Dodd S. L. , Lu B.-S. , Druzhinina I. S. . ( 2006b; ). Hypocrea rufa/Trichoderma viride: a reassessment, and description of five closely related species with and without warted conidia. . Stud Mycol 56:, 135–177. [CrossRef] [PubMed]
    [Google Scholar]
  26. Jaklitsch W. M. , Kubicek C. P. , Druzhinina I. S. . ( 2008; ). Three European species of Hypocrea with reddish brown stromata and green ascospores. . Mycologia 100:, 796–815. [CrossRef] [PubMed]
    [Google Scholar]
  27. Klein D. , Eveleigh D. E. . ( 1998; ). Ecology of Trichoderma . . In Trichoderma & Gliocladium, vol. 1, pp. 57–73. Edited by Harman G. E. , Kubicek C. P. . . London:: Taylor & Francis;.
    [Google Scholar]
  28. Komon-Zelazowska M. , Bissett J. , Zafari D. , Hatvani L. , Manczinger L. , Woo S. , Lorito M. , Kredics L. , Kubicek C. P. , Druzhinina I. S. . ( 2007; ). Genetically closely related but phenotypically divergent Trichoderma species cause green mold disease in oyster mushroom farms worldwide. . Appl Environ Microbiol 73:, 7415–7426. [CrossRef] [PubMed]
    [Google Scholar]
  29. Kopchinskiy A. G. , Komon M. , Kubicek C. P. , Druzhinina I. S. . ( 2005; ). Tricho blast: a multiloci database for Trichoderma and Hypocrea identification. . Mycol Res 109:, 658–660. [CrossRef]
    [Google Scholar]
  30. Kraus G. F. , Druzhinina I. S. , Gams W. , Bissett J. , Zafari D. , Szakacs G. , Koptchinski A. , Prillinger H. , Zare R. , Kubicek C. P. . ( 2004; ). Trichoderma brevicompactum sp. nov. . Mycologia 96:, 1059–1073. [CrossRef] [PubMed]
    [Google Scholar]
  31. Kubicek C. P. , Komon-Zelazowska M. , Druzhinina I. S. . ( 2008; ). Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. . J Zhejiang Univ Sci B 9:, 753–763. [CrossRef] [PubMed]
    [Google Scholar]
  32. Kubicek C. P. , Herrera-Estrella A. , Seidl-Seiboth V. , Martinez D. A. , Druzhinina I. S. , Thon M. , Zeilinger S. , Casas-Flores S. , Horwitz B. A. . & other authors ( 2011; ). Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma . . Genome Biol 12:, R40. [CrossRef] [PubMed]
    [Google Scholar]
  33. Lim Y. W. , Kim B. K. , Kim C. , Jung H. S. , Kim B. S. , Lee J. H. , Chun J. . ( 2010; ). Assessment of soil fungal communities using pyrosequencing. . J Microbiol 48:, 284–289. [CrossRef] [PubMed]
    [Google Scholar]
  34. Linhart C. , Shamir R. . ( 2005; ). The degenerate primer design problem: theory and applications. . J Comput Biol 12:, 431–456. [CrossRef] [PubMed]
    [Google Scholar]
  35. Lorito M. , Woo S. L. , Harman G. E. , Monte E. . ( 2010; ). Translational research on Trichoderma: from ’omics to the field. . Annu Rev Phytopathol 48:, 395–417. [CrossRef] [PubMed]
    [Google Scholar]
  36. Martinez D. , Berka R. M. , Henrissat B. , Saloheimo M. , Arvas M. , Baker S. E. , Chapman J. , Chertkov O. , Coutinho P. M. . & other authors ( 2008; ). Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). . Nat Biotechnol 26:, 553–560. [CrossRef] [PubMed]
    [Google Scholar]
  37. Meincke R. , Weinert N. , Radl V. , Schloter M. , Smalla K. , Berg G. . ( 2010; ). Development of a molecular approach to describe the composition of Trichoderma communities. . J Microbiol Methods 80:, 63–69. [CrossRef] [PubMed]
    [Google Scholar]
  38. Migheli Q. , Balmas V. , Komoń-Zelazowska M. , Scherm B. , Fiori S. , Kopchinskiy A. G. , Kubicek C. P. , Druzhinina I. S. . ( 2009; ). Soils of a Mediterranean hot spot of biodiversity and endemism (Sardinia, Tyrrhenian Islands) are inhabited by pan-European, invasive species of Hypocrea/Trichoderma . . Environ Microbiol 11:, 35–46. [CrossRef]
    [Google Scholar]
  39. Mulaw T. B. , Kubicek C. P. , Druzhinina I. S. . ( 2010; ). The rhizosphere of Coffea arabica in its native highland forests of Ethiopia is associated with a distinguished diversity of Trichoderma . . Diversity 2:, 527–549. [CrossRef]
    [Google Scholar]
  40. Nemcovic M. , Jakubíková L. , Víden I. , Farkas V. . ( 2008; ). Induction of conidiation by endogenous volatile compounds in Trichoderma spp. . FEMS Microbiol Lett 284:, 231–236. [CrossRef] [PubMed]
    [Google Scholar]
  41. Nicholas K. B. , Nicholas H. B. Jr , . ( 1997; ). Genedoc: a tool for editing and annotating multiple sequence alignments. http://www.psc.edu/biomed/genedoc.
  42. Overton B. E. , Stewart E. L. , Geiser D. M. , Jaklitsch W. M. . ( 2006; ). Systematics of Hypocrea citrina and related taxa. . Stud Mycol 56:, 1–38. [CrossRef] [PubMed]
    [Google Scholar]
  43. Robertson G. P. , Coleman D. C. , Bledsoe C. S. . ( 1999; ). Standard Soil Methods for Long-Term Ecological Research. Oxford:: Cambridge University press;.
    [Google Scholar]
  44. Rossmann A. Y. , Samuels G. J. , Rogerson C. T. , Lowen R. . ( 1999; ). Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). . Stud Mycol 42:, 1–83.
    [Google Scholar]
  45. Samuels G. J. . ( 2005; ). Changes in taxonomy, occurrence of the sexual stage and ecology of Trichoderma spp. . Phytopathology 96:, 195–220. [CrossRef]
    [Google Scholar]
  46. Samuels G. J. , Pardo-Schultheiss R. A. , Hebbar K. P. , Lumsden R. D. , Bastos C. N. , Costa J. C. , Bezerra J. L. . ( 2000; ). Trichoderma stromaticum sp. nov., a parasite of the cacao witches broom pathogen. . Mycol Res 104:, 760–764. [CrossRef]
    [Google Scholar]
  47. Samuels G. J. , Suarez C. , Solis K. , Holmes K. A. , Thomas S. E. , Ismaiel A. , Evans H. C. . ( 2006a; ). Trichoderma theobromicola and T. paucisporum: two new species isolated from cacao in South America. . Mycol Res 110:, 381–392. [CrossRef] [PubMed]
    [Google Scholar]
  48. Samuels G. J. , Dodd S. L. , Lu B.-S. , Petrini O. , Schroers H. J. , Druzhinina I. S. . ( 2006b; ). The Trichoderma koningii aggregate species. . Stud Mycol 56:, 67–133. [CrossRef] [PubMed]
    [Google Scholar]
  49. Samuels G. J. , Ismaiel A. , Bon M.-C. , De Respinis S. , Petrini O. . ( 2010; ). Trichoderma asperellum sensu lato consists of two cryptic species. . Mycologia 102:, 944–966. [CrossRef] [PubMed]
    [Google Scholar]
  50. Thompson J. D. , Gibson T. J. , Plewniak F. , Jeanmougin F. , Higgins D. G. . ( 1997; ). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. . Nucleic Acids Res 25:, 4876–4882. [CrossRef] [PubMed]
    [Google Scholar]
  51. Tockner K. , Schiemer F. , Ward J. V. . ( 1998; ). Conservation by restoration: the management concept for a river-floodplain system on the Danube river in Austria. . Aquatic Conserv Mar Freshw Ecosyst 8:, 71–86. [CrossRef]
    [Google Scholar]
  52. White T. J. , Bruns T. , Lee S. , Taylor J. W. . ( 1990; ). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. . In PCR protocols: a guide to methods and applications, pp. 315–322. Edited by Innis M. A. , Gelfand D. H. , Sninsky J. J. , White T. J. . . New York:: Academic Press;.
    [Google Scholar]
  53. Wuczkowski M. , Druzhinina I. , Gherbawy Y. , Klug B. , Prillinger H. J. , Kubicek C. P. . ( 2003; ). Species pattern and genetic diversity of Trichoderma in a mid-European, primeval floodplain-forest. . Microbiol Res 158:, 125–133. [CrossRef] [PubMed]
    [Google Scholar]
  54. Zachow C. , Berg C. , Müller H. , Meincke R. , Komon-Zelazowska M. , Druzhinina I. S. , Kubicek C. P. , Berg G. . ( 2009; ). Fungal diversity in the rhizosphere of endemic plant species of Tenerife (Canary Islands): relationship to vegetation zones and environmental factors. . ISME J 3:, 79–92. [CrossRef] [PubMed]
    [Google Scholar]
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