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Journal of Zhejiang University SCIENCE B 2008 Vol.9 No.10 P.753~763


Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity

Author(s):  Christian P. KUBICEK, Monika KOMON-ZELAZOWSKA, Irina S. DRUZHININA

Affiliation(s):  Institute of Chemical Engineering, Research Area Gene Technology and Applied Biochemistry, Vienna University of Technology, Getreidemarkt 9/E1665, A-1060 Vienna, Austria

Corresponding email(s):   ckubicek@mail.zserv.tuwien.ac.at

Key Words:  Hypocrea/Trichoderma, Biogeography, Biodiversity, Facultative human opportunists, Peptaibols, Mushroom pathogens

Christian P. KUBICEK, Monika KOMON-ZELAZOWSKA, Irina S. DRUZHININA. Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity[J]. Journal of Zhejiang University Science B, 2008, 9(10): 753~763.

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publisher="Zhejiang University Press & Springer",

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%T Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity
%A Christian P. KUBICEK
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%D 2008
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B0860015

T1 - Fungal genus Hypocrea/Trichoderma: from barcodes to biodiversity
A1 - Christian P. KUBICEK
J0 - Journal of Zhejiang University Science B
VL - 9
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SP - 753
EP - 763
%@ 1673-1581
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PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B0860015

Hypocrea/Trichoderma is a genus of soil-borne or wood-decaying fungi containing members important to mankind as producers of industrial enzymes and biocontrol agents against plant pathogens, but also as opportunistic pathogens of immunocompromised humans and animals, while others can cause damage to cultivated mushroom. With the recent advent of a reliable, BarCode-aided identification system for all known taxa of Trichoderma and Hypocrea, it became now possible to study some of the biological fundamentals of the diversity in this fungal genus in more detail. In this article, we will therefore review recent progress in (1) the understanding of the geographic distribution of individual taxa; (2) mechanisms of speciation leading to development of mushroom diseases and facultative human mycoses; and (3) the possible correlation of specific traits of secondary metabolism and molecular phylogeny.

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article


[1] Arisan-Atac, I., Heidenreich, E., Kubicek, C.P., 1995. Randomly amplified polymorphic DNA fingerprinting identifies subgroups of Trichoderma viride and other Trichoderma sp. capable of chestnut blight biocontrol. FEMS Microbiol. Lett., 126(3):249-256.

[2] Benedetti, E., Bavoso, A., Di Blasio, B., Pavone, V., Pedone, C., Toniolo, C., Bonora, G.M., 1982. Peptaibol antibiotics: a study on the helical structure of the two sequences of emerimicins III and IV. Proc. Natl. Acad. Sci. USA, 79(24):7951-7954.

[3] Brückner, H., Graf, A., 1983. Paracelsin, a peptid antibiotic containing alpha-aminoisobutyric acid, isolated from Trichoderma reesei Simmons. Part A. Experientia, 39(5):528-530.

[4] Brückner, H., Graf, H., Bokel, M., 1984. Paracelsin: characterization by NMR spectroscopy and circular dichroism, and hemolytic properties of a peptaibol antibiotic from the cellulolytically active mold Trichoderma reesei Simmons. Part B. Experientia, 40(11):1189-1197.

[5] Burt, A., Carter, D.A., Koenig, G., White, T.J., Taylor, J.W., 1996. Molecular markers reveal cryptic sex in the human pathogen Coccidioides immitis. Proc. Natl. Acad. Sci. USA, 93(2):770-773.

[6] Castle, A., Speranzini, D., Rghei, N., Alm, G., Rinker, D., Bissett, J., 1998. Morphological and molecular identification of Trichoderma isolates on North American mushroom farms. Appl. Environ. Microbiol., 64:133-137.

[7] Dababat, A.A., Sikora, R.A., Hauschild, R., 2006. Use of Trichoderma harzianum and Trichoderma viride for the biological control of Meloidogyne incognita on tomato. Commun. Agric. Appl. Biol. Sci., 71:953-961.

[8] Danielson, R.M., Davey, C.B., 1973. The abundance of Trichoderma propagules and the distribution of species in forest soils. Soil Biol. Biochem., 5(5):485-494.

[9] Degenkolb, T., Gräfenhan, T., Berg, A., Nirenberg, H.I., Gams, W., Brückner, H., 2006a. Peptaibiomics: screening for polypeptide antibiotics (peptaibiotics) from plant-protective Trichoderma species. Chem. Biodivers., 3(6):593-610.

[10] Degenkolb, T., Gräfenhan, A., Nirenberg, H.I., Gams, W., Brückner, H., 2006b. Trichoderma brevicompactum complex: rich source of novel and recurrent plant-protective polypeptide antibiotics (peptaibiotics). J. Agric. Food Chem., 54(19):7047-7061.

[11] Degenkolb, T., von Döhren, H., Nielsen, K.F., Samuels, G.J., Brückner, H., 2008. Recent advances and future prospects in peptaibiotics, hydrophobin, and mycotoxin research, and their importance for chemotaxonomy of Trichoderma and Hypocrea. Chem. Biodivers., 5(5):671-680.

[12] Dodd, S.L., Lieckfeldt, E., Samuels, G.J., 2003. Hypocrea atroviridis sp. nov., the teleomorph of Trichoderma atroviride. Mycologia, 95(1):27-40.

[13] Druzhinina, I.S., Kopchinskiy, A.G., 2006. TrichOKEY v. 2— A DNA Oligonucleotide BarCode Program for the Identification of Multiple Sequences of Hypocrea and Trichoderma. In: Meyer, W., Pearce, C. (Eds.), International Proceedings of the 8th International Mycological Congress. Cairns, Australia, Medimond, Bologna, Italy.

[14] Druzhinina, I.S., Kopchinskiy, A.G., Komon, M., Bissett, J., Szakacs, G., Kubicek, C.P., 2005. An oligonucleotide barcode for species identification in Trichoderma and Hypocrea. Fungal Genet. Biol., 42(10):813-828.

[15] Druzhinina, I.S., Komoń-Zelazowska, M., Kredics, L., Hatvani, L., Antal, Z., Belayneh, T., Kubicek, C.P., 2008. Different reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable to cause invasive mycoses of humans. Microbiology UK, in press.

[16] Finlay, B.J., 2002. Global dispersal of free-living microbial eukaryotic species. Science, 296(5570):1061-1063.

[17] Furukawa, H., Kusne, S., Sutton, D.A., Manez, R., Carrau, R., Nichols, L., Abu-Elmagd, K., Skedros, D., Todo, D., Rinaldi, M.G., 1998. Acute invasive sinusitis due to Trichoderma longibrachiatum in a liver and small bowel transplant recipient. Clin. Infect. Dis., 26(2):487-489.

[18] Geiser, D.M., Pitt, J.I., Taylor, J.W., 1998. Cryptic speciation and recombination in the aflatoxin producing fungus Aspergillus flavus. Proc. Natl. Acad. Sci. USA, 95(1):388-393.

[19] Gherbawy, Y., Druzhinina, I., Shaban, G.M., Wuczkowski, M., Yaser, M., El-Naghy, M.A., Prillinger, H.J., Kubicek, C.P., 2004. Trichoderma populations from alkaline agricultural soil in the Nile valley, Egypt, consist of only two species. Mycol. Prog., 3(3):211-218.

[20] Goswami, J., Pandey, R.K., Tewari, J.P., Goswami, B.K., 2008. Management of root knot nematode in tomato through application of fungal antagonists, Acremonium strictum and Trichoderma harzianum. J. Environ. Sci. Health B, 43(3):237-240.

[21] Grill, A., Casula, P., Lecis, R., Menken, S.B.J., 2006. Endemism in Sardinia. In: Weiss, S., Ferrand, N. (Eds.), Phylogeography of Southern European Refugia. Springer, Dordrecht, the Netherlands, p.273-296.

[22] Harman, G.E., Howell, C.R., Viterbo, A., Chet, I., Lorito, M., 2004. Trichoderma species-opportunistic, avirulent plant symbionts. Nature Rev. Microbiol., 2(1):43-56.

[23] Hatvani, L., Antal, Z., Manczinger, A., Szekeres, A., Druzhinina, I.S., Kubicek, C.P., Nagy, A., Nagy, E., Vágvölgyi, C., Kredics, L., 2007. Green mould diseases of Agaricus and Pleurotus spp. are caused by related but phylogenetically different Trichoderma species. Phytopathology, 97(4):532-537.

[24] Hennequin, C., Chouaki, T., Pichon, J.C., Strunski, V., Raccurt, C., 2000. Otitis externa due to Trichoderma longi-brachiatum. Eur. J. Clin. Microbiol. Infect. Dis., 19(8):641-642.

[25] ISTH (International Subcomission on Trichoderma and Hypocrea Taxonomy), 2008. ISTH.info—a Website of Trichoderma DNA BarCode [WWW]. Irina Druzhinina & Alexey Kopchinskiy. Available from http://www.isth.info (accessed 20/08/2008).

[26] Kasuga, T., White, T.J., Koenig, J., McEwen, J., Castaneda, E., Lacaz, C.D.S., Heins-Vaccari, E.M., De Freitas, R.S., Zan-Cope-Oliveira, R.M., Qin, Z., et al., 2003. Phylogeography of the fungal pathogen Histoplasma capsulatum. Mol. Ecol., 12(12):3383-3401.

[27] Klein, D., Eveleigh, E., 1998. Ecology of Trichoderma. In: Kubicek, C.P., Harman, G.E. (Eds.), Trichoderma and Gliocladium. Basic Biology, Taxonomy and Genetics. Taylor & Francis Ltd., London, UK, p.57-74.

[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 world-wide green mould disease in oyster mushroom farms. Appl. Environ. Microbiol., 73(22):7415-7426.

[29] Kopchinskiy, A.G., Komoń, M., Kubicek, C.P., Druzhinina, I.S., 2005. TrichoBLAST: a multiloci database of phylogenetic markers for Trichoderma and Hypocrea powered by sequence diagnosis and similarity search tools. Mycol. Res., 109(6):658-660.

[30] Koufopanou, V., Burt, A., Szaro, T., Taylor, J.W., 2001. Gene genealogies, cryptic species, and molecular evolution in the human pathogen Coccidioides immitis and relatives (Ascomycota, Onygenales). Mol. Biol. Evol., 18:1246-1258.

[31] Kraus, G., Druzhinina, I., Bissett, J., Prillinger, H.J., Szakacs, G., Gams, W., Kubicek, C.P., 2004. Trichoderma brevicompactum sp. nov. Mycologia, 96(5):1059-1073.

[32] Kredics, L., Antal, Z., Doczi, I., Manczinger, L., Kevei, F., Nagy, E., 2003. Clinical importance of the genus Trichoderma. A review. Acta Microbiol. Immunol. Hung., 50(2-3):105-117.

[33] Kubicek, C.P., Bölzlbauer, U.M., Kovacs, W., Mach, R.L., Kuhls, K., Lieckfeldt, U., Börner, T., Samuels, G.J., 1996. Cellulase formation by species of Trichoderma sect. Longibrachiatum and of Hypocrea spp. with anamorphs referable to Trichoderma sect. Longibrachiatum. Fungal Genet. Biol., 20(2):105-114.

[34] Kubicek, C.P., Bissett, J., Kullnig-Gradinger, C.M., Druzhinina, I.S., Szakacs, G., 2003. Genetic and metabolic diversity of Trichoderma: a case study on South-East Asian isolates. Fungal Genet. Biol., 38(3):310-317.

[35] Kuhls, K., Lieckfeldt, E., Börner, T., Guého, E., 1999. Molecular re-identification of human pathogenic Trichoderma isolates as Trichoderma longibrachiatum and Trichoderma citrinoviride. Med. Mycol., 37(1):25-33.

[36] Kullnig, C., Szakacs, G., Kubicek, C.P., 2000. Molecular identification of Trichoderma species from Russia, Siberia and the Himalaya. Mycol. Res., 104(9):1117-1125.

[37] Kyalo, G., Affokpon, A., Coosemans, J., Coynes, D.L., 2007. Biological control effects of Pochonia chlamysdosporia and Trichoderma isolates from Benin (West-Africa) on root-knot nematodes. Commun. Agric. Appl. Biol. Sci., 72:219-223.

[38] Médail, F., Quézal, P., 1999. Biodiversity hotspots in the Mediterranean Basin: setting global conservation priorities. Conserv. Biol., 13(6):1510-1513.

[39] Migheli, Q., Balmas, V., Komoń-Zelazowska, M., Scherm, B., Caria, R., Kopchinskiy, A., Kubicek, C.P., Druzhinina, I.S., 2008. Soils of a Mediterranean hotspot of biodiversity and endemism (Sardinia, Tyrrhenian Islands) are inhabited by pan-European and likely invasive species of Hypocrea/Trichoderma. Environ. Microbiol., Sept. 1. 2008 [Epub ahead of print].

[40] Milgroom, M.G., 1996. Recombination and the multilocus structure of fungal populations. Annu. Rev. Phytopathol., 34(1):457-477.

[41] Munoz, F.M., Demmler, G.J., Travis, W.R., Ogden, A.K., Rossmann, S.N., Rinaldi, M.G., 1997. Trichoderma longibrachiatum infection in a pediatric patient with aplastic anemia. J. Clin. Microbiol., 35:499-503.

[42] Muthumeenakshi, S., Mills, P.R., Brown, A.E., Seaby, D.A., 1994. Intraspecific molecular variation among Trichoderma harzianum isolates colonizing mushroom compost in the British Isles. Microbiology UK, 140:769-777.

[43] Myoken, Y., Sugata, T., Fujita, Y., Asaoku, H., Fujihara, M., Mikami, Y., 2002. Fatal necrotizing stomatitis due to Trichoderma longibrachiatum in a neutropenic patient with malignant lymphoma: a case report. Int. J. Oral Maxillofac. Surg., 31(6):688-691.

[44] Nagy, V., Seidl, V., Szakacs, G., Komon-Zelazowska, M., Kubicek, C.P., Druzhinina, I.S., 2007. Application of DNA BarCodes for screening of industrially important fungi: the haplotype of Trichoderma harzianum sensu stricto indicates superior chitinase formation. Appl. Environ. Microbiol., 73(21):7048-7058.

[45] Nelson, E.E., 1982. Occurrence of Trichoderma in a douglas-fir soil. Mycologia, 74(2):280-284.

[46] Neuhof, T., Dieckmann, R., Druzhinina, I.S., Kubicek, C.P., von Döhren, H., 2007. Intact-Cell MALDI-TOF mass spectrometry analysis of peptaibol formation by the genus Trichoderma: can molecular phylogenic knowledge predict peptaibol structures? Microbiology, 153(10):3417-3437.

[47] Nielsen, K., Heitman, J., 2007. Sex and virulence of human pathogenic fungi. Adv. Genet., 57:143-173.

[48] Normark, B.B., Judson, O.P., Morgan, N.A., 2003. Genomic signatures of ancient asexual lineages. Biol. J. Linn. Soc. Lond., 79(1):69-84.

[49] Ospina-Giraldo, M.D., Royse, D.J., Chen, X., Romaine, C.P., 1999. Molecular phylogenetic analysis of biological control strains of Trichoderma harzianum and other biotypes of Trichoderma spp. associated with mushroom green mold. Phytopathology, 89(4):308-313.

[50] Paoletti, M., Rydholm, C., Schwier, E.U., Anderson, M.J., Szakacs, G., Lutzoni, F., Debeaupuis, J.P., Latgé, J.P., Denning, D.W., Dyer, P.S., 2005. Evidence for sexuality in the opportunistic fungal pathogen Aspergillus fumigatus. Curr. Biol., 15(13):1242-1248.

[51] Park, M.S., Bae, K.S., Yu, S.H., 2006. Two new species of Trichoderma associated with green mold of oyster mushroom cultivation in Korea. Mycobiology, 34:11-113.

[52] Rossmann, A.Y., Samuels, G.J., Rogerson, C.T., Lowen, R., 1999. Genera of Bionectriaceae, Hypocreaceae and Nectriaceae (Hypocreales, Ascomycetes). Stud. Mycology, 42:248.

[53] Samuels, G.J., Dodd, S.L., Gams, W., Castlebury, L.A., Petrini, O., 2002. Trichoderma species associated with the green mold epidemic of commercially grown Agaricus bisporus. Mycologia, 94(1):146-170.

[54] Samuels, G.J., Dodd, S., Lu, B., Petrini, O., Schroers, H.J., Druzhinina, I.S., 2006. The Trichoderma koningii morphological species. Stud. Mycol., 56(1):67-133.

[55] Seaby, D., 1998. Trichoderma as a Weed and Pathogen in Mushroom Cultivation. In: Harman, G.E., Kubicek, C.P. (Eds.), Trichoderma and Gliocladium. Vol. 2. Enzymes, Biological Control and Commercial Applications. Taylor and Francis Ltd., London, p.267-283.

[56] Szekeres, A., Leitgeb, B., Kredics, L., Antal, Z., Hatvani, L., Manczinger, L., Vágvölgyi, C., 2005. Peptaibols and related peptaibiotics of Trichoderma. Acta Microbiol. Immunol. Hung., 52(2):137-168.

[57] Turner, D., Kovacs, W., Kuhls, K., Lieckfeldt, E., Peter, B., Arisan-Atac, I., Strauss, J., Samuels, G.J., Börner, T., Kubicek, C.P., 1997. Biogeography and phenotypic variation in Trichoderma sect. Longibrachiatum and associated Hypocrea species. Mycol. Res., 101(4):449-459.

[58] Vizcaíno, J.A., Cardoza, R.E., Dubost, L., Bodo, B., Gutièrrez, S., Monte, E., 2006. Detection of peptaibols and cloning of a putative peptaibol synthetase gene from Trichoderma harzianum CECT 2413. Folia Microbiol., 51(2):114-120.

[59] Walsh, T.J., Groll, A.H., 1999. Emerging fungal pathogens: evolving challenges to immunocompromised patients for the twenty-first century. Transplant Infect. Dis., 1(4):247-261.

[60] Whitmore, L., Wallace, B.A., 2004. The peptaibol database: a database for sequences and structures of naturally occurring peptaibols. Nucleic. Acids Res., 32(90001):D593-D594.

[61] Widden, P., Abitbol, J.J., 1980. Seasonality of Trichoderma species in a spruce forest soil. Mycologia, 72(4):775-784.

[62] Wiest, A., Grzegorski, D., Xu, B.W., Goulard, C., Rebuffat, S., Ebbole, D.J., Bodo, B., Kenerley, C., 2002. Identification of peptaibols from Trichoderma virens and cloning of a peptaibol synthetase. J. Biol. Chem., 277(23):20862-20868.

[63] 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(2):125-133.

[64] Zachow, C., Berg, C., Müller, H., Meincke, R., Komon-Zelazowska, M., Druzhinina, I.S., Kubicek, C.P., Berg, G., 2008. Fungal biodiversity in the soils/ rhizospheres of Tenerife (Canary Islands): relationship to vegetation zones and environmental factors. ISME J., in press.

[65] Zhang, C., Druzhinina, I.S., Kubicek, C.P., Xu, T., 2005. Trichoderma biodiversity in China: evidence for a North to South distribution of species in East Asia. FEMS Microbiol. Lett., 251(2):251-257.

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