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.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.052555-0
2012-01-01
2020-12-05
Loading full text...

Full text loading...

/deliver/fulltext/micro/158/1/69.html?itemId=/content/journal/micro/10.1099/mic.0.052555-0&mimeType=html&fmt=ahah

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 Microbiol76:7259–7267 [CrossRef][PubMed]
    [Google Scholar]
  2. Batjes N. H.. ( 1996;). Total carbon and nitrogen in the soils of the world. Eur J Soil Sci47:151–163 [CrossRef]
    [Google Scholar]
  3. Betina V., Farkas V.. ( 1998;). Sporulation and light-induced development in Trichoderma . Trichoderma & Gliocladiumvol. 175–94 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 Phytol184:449–456 [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 Evol27:302–313 [CrossRef][PubMed]
    [Google Scholar]
  7. 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 Biol42:813–828 [CrossRef][PubMed]
    [Google Scholar]
  8. Druzhinina I. S., Kopchinskiy A. G., Kubicek C. P.. ( 2006;). The first 100 Trichoderma species characterized by molecular data. Mycoscience47:55–64 [CrossRef]
    [Google Scholar]
  9. 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. Microbiology154:3447–3459 [CrossRef][PubMed]
    [Google Scholar]
  10. 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 ONE5:e9191 [CrossRef][PubMed]
    [Google Scholar]
  11. 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 Biol10:94 [CrossRef][PubMed]
    [Google Scholar]
  12. 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 Microbiol9:749–759 [CrossRef][PubMed]
    [Google Scholar]
  13. FAO ( 1998;). World Reference Base for Soil Resources Rome: Food and Agriculture Organization of the United Nations;
    [Google Scholar]
  14. Friedl M. A., Kubicek C. P., Druzhinina I. S.. ( 2008;). Carbon source dependence and photostimulation of conidiation in Hypocrea atroviridis . Appl Environ Microbiol74:245–250 [CrossRef][PubMed]
    [Google Scholar]
  15. Gazis R., Rehner S., Chaverri P.. ( 2011;). Species delimitation in fungal endophyte diversity studies and its implications in ecological and biogeographic inferences. Mol Ecol20:3001–3013 [CrossRef][PubMed]
    [Google Scholar]
  16. 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 Methods69:86–92 [CrossRef][PubMed]
    [Google Scholar]
  17. Harman G. E., Howell C. R., Viterbo A., Chet I., Lorito M.. ( 2004;). Trichoderma species – opportunistic, avirulent plant symbionts. Nature Rev Microbiol2:43–56 [CrossRef][PubMed]
    [Google Scholar]
  18. Hawksworth D. L.. ( 1991;). The fungal dimension of biodiversity: magnitude, significance, and conservation. Mycol Res95:641–655 [CrossRef]
    [Google Scholar]
  19. Hoyos-Carvajal L., Orduz S., Bissett J.. ( 2009;). Genetic and metabolic biodiversity of Trichoderma from Colombia and adjacent neotropic regions. Fungal Genet Biol46:615–631 [CrossRef][PubMed]
    [Google Scholar]
  20. Jaklitsch W. M.. ( 2009;). European species of Hypocrea Part I. The green-spored species. Stud Mycol63:1–91 [CrossRef][PubMed]
    [Google Scholar]
  21. Jaklitsch W. M.. ( 2011;). European species of Hypocrea. Part II: species with hyaline ascospores. Fungal Divers48:1–250[PubMed][CrossRef]
    [Google Scholar]
  22. 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 . Mycologia97:1365–1378 [CrossRef][PubMed]
    [Google Scholar]
  23. 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. Mycologia98:499–513 [CrossRef][PubMed]
    [Google Scholar]
  24. 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 Mycol56:135–177 [CrossRef][PubMed]
    [Google Scholar]
  25. Jaklitsch W. M., Kubicek C. P., Druzhinina I. S.. ( 2008;). Three European species of Hypocrea with reddish brown stromata and green ascospores. Mycologia100:796–815 [CrossRef][PubMed]
    [Google Scholar]
  26. Klein D., Eveleigh D. E.. ( 1998;). Ecology of Trichoderma . Trichoderma & Gliocladiumvol. 157–73 Harman G. E., Kubicek C. P.. London: Taylor & Francis;
    [Google Scholar]
  27. 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 Microbiol73:7415–7426 [CrossRef][PubMed]
    [Google Scholar]
  28. Kopchinskiy A. G., Komon M., Kubicek C. P., Druzhinina I. S.. ( 2005;). Tricho blast: a multiloci database for Trichoderma and Hypocrea identification. Mycol Res109:658–660 [CrossRef]
    [Google Scholar]
  29. 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. Mycologia96:1059–1073 [CrossRef][PubMed]
    [Google Scholar]
  30. Kubicek C. P., Komon-Zelazowska M., Druzhinina I. S.. ( 2008;). Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity. J Zhejiang Univ Sci B9:753–763 [CrossRef][PubMed]
    [Google Scholar]
  31. 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 Biol12:R40 [CrossRef][PubMed]
    [Google Scholar]
  32. 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 Microbiol48:284–289 [CrossRef][PubMed]
    [Google Scholar]
  33. Linhart C., Shamir R.. ( 2005;). The degenerate primer design problem: theory and applications. J Comput Biol12:431–456 [CrossRef][PubMed]
    [Google Scholar]
  34. Lorito M., Woo S. L., Harman G. E., Monte E.. ( 2010;). Translational research on Trichoderma: from ’omics to the field. Annu Rev Phytopathol48:395–417 [CrossRef][PubMed]
    [Google Scholar]
  35. 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 Biotechnol26:553–560 [CrossRef][PubMed]
    [Google Scholar]
  36. 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 Methods80:63–69 [CrossRef][PubMed]
    [Google Scholar]
  37. 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 Microbiol11:35–46 [CrossRef]
    [Google Scholar]
  38. 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 . Diversity2:527–549 [CrossRef]
    [Google Scholar]
  39. Nemcovic M., Jakubíková L., Víden I., Farkas V.. ( 2008;). Induction of conidiation by endogenous volatile compounds in Trichoderma spp. FEMS Microbiol Lett284:231–236 [CrossRef][PubMed]
    [Google Scholar]
  40. Nicholas K. B., Nicholas H. B. Jr. ( 1997;).http://www.psc.edu/biomed/genedoc
  41. Overton B. E., Stewart E. L., Geiser D. M., Jaklitsch W. M.. ( 2006;). Systematics of Hypocrea citrina and related taxa. Stud Mycol56:1–38 [CrossRef][PubMed]
    [Google Scholar]
  42. Robertson G. P., Coleman D. C., Bledsoe C. S.. ( 1999;). Standard Soil Methods for Long-Term Ecological Research Oxford: Cambridge University press;
    [Google Scholar]
  43. Rossmann A. Y., Samuels G. J., Rogerson C. T., Lowen R.. ( 1999;). Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud Mycol42:1–83
    [Google Scholar]
  44. Samuels G. J.. ( 2005;). Changes in taxonomy, occurrence of the sexual stage and ecology of Trichoderma spp. Phytopathology96:195–220 [CrossRef]
    [Google Scholar]
  45. 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 Res104:760–764 [CrossRef]
    [Google Scholar]
  46. 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 Res110:381–392 [CrossRef][PubMed]
    [Google Scholar]
  47. Samuels G. J., Dodd S. L., Lu B.-S., Petrini O., Schroers H. J., Druzhinina I. S.. ( 2006b;). The Trichoderma koningii aggregate species. Stud Mycol56:67–133 [CrossRef][PubMed]
    [Google Scholar]
  48. Samuels G. J., Ismaiel A., Bon M.-C., De Respinis S., Petrini O.. ( 2010;). Trichoderma asperellum sensu lato consists of two cryptic species. Mycologia102:944–966 [CrossRef][PubMed]
    [Google Scholar]
  49. 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 Res25:4876–4882 [CrossRef][PubMed]
    [Google Scholar]
  50. 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 Ecosyst8:71–86 [CrossRef]
    [Google Scholar]
  51. White T. J., Bruns T., Lee S., Taylor J. W.. ( 1990;). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications315–322 Innis M. A., Gelfand D. H., Sninsky J. J., White T. J.. New York: Academic Press;
    [Google Scholar]
  52. 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 Res158:125–133 [CrossRef][PubMed]
    [Google Scholar]
  53. 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 J3:79–92 [CrossRef][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.052555-0
Loading
/content/journal/micro/10.1099/mic.0.052555-0
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error