The Trichoderma Brevicompactum Clade: a Separate Lineage with New Species, New Peptaibiotics, and Mycotoxins
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Mycol Progress (2008) 7:177–219 DOI 10.1007/s11557-008-0563-3 ORIGINAL ARTICLE The Trichoderma brevicompactum clade: a separate lineage with new species, new peptaibiotics, and mycotoxins Thomas Degenkolb & Ralf Dieckmann & Kristian Fog Nielsen & Tom Gräfenhan & Christoph Theis & Doustmorad Zafari & Priscila Chaverri & Adnan Ismaiel & Hans Brückner & Hans von Döhren & Ulf Thrane & Orlando Petrini & Gary J. Samuels Received: 8 January 2008 /Revised: 27 March 2008 /Accepted: 8 April 2008 /Published online: 5 July 2008 # German Mycological Society and Springer 2008 Abstract The Brevicompactum clade is recognized as a viously reported as T. harzianum (ATCC 90237), T. viride separate lineage in Trichoderma/Hypocrea. This includes T. (NRRL 3199) or Hypocrea sp. (F000527, CBS 113214) to brevicompactum and the new species T. arundinaceum, T. produce trichothecenes are reidentified as T. arundinaceum. turrialbense, T. protrudens and Hypocrea rodmanii. The The Brevicompactum clade is not closely related to species closest relative of the Brevicompactum clade is the Lutea that have biological application. clade. With the exception of H. rodmanii, all members of this clade produce the simple trichothecene-type toxins Keywords Hypocrea . Hypocreales . Hypocreaceae . harzianum A or trichodermin. All members of the clade Systematics . Hydrophobins . Trichothecene . Harzianum A . produce peptaibiotics, including alamethicins. Strains pre- Trichodermin . Endophyte . MALDI-TOF. Biocontrol Taxonomic novelties Hypocrea rodmanii Samuels & Chaverri, Trichoderma arundinaceum Zafari, Gräfenhan & Samuels, Trichoderma protrudens Samuels & Chaverri, Trichoderma turrialbense Samuels, Degenkolb, K.F. Nielsen & Gräfenhan. : : T. Degenkolb C. Theis H. Brückner D. Zafari Interdisciplinary Research Centre for Biosystems, Faculty of Agriculture, Bu Ali Sina University, Land Use and Nutrition (IFZ), Department of Food Sciences, Hamadan, Iran Institute of Nutritional Science, University of Giessen, Heinrich-Buff-Ring 26-32, P. Chaverri 35392 Giessen, Germany Department of Biology, Howard University, : 415 College Street NW, R. Dieckmann H. von Döhren Washington, DC 20059, USA Technische Universität Berlin, Institut für Chemie, FG Biochemie und Molekulare Biologie, Franklinstraße 29, A. Ismaiel : G. J. Samuels (*) 10587 Berlin, Germany United States Department of Agriculture, ARS, : Systematic Mycology & Microbiology Laboratory, K. F. Nielsen U. Thrane B-011a, Rm. 304, 10300 Baltimore Ave., Center for Microbial Biotechnology (CMB), BioCentrum, Beltsville, MD 20705, USA Technical University of Denmark, e-mail: [email protected] Building 221, 2800 Lyngby, Denmark O. Petrini T. Gräfenhan Repubblica e Cantone Ticino, Eastern Cereals and Oilseeds Research Centre, Istituto Cantonale di Microbiologia, William Saunders Building, Agriculture and Agri-Food Canada, Via Mirasole 22A, Ottawa, ON K1A OC6, Canada 6500 Bellinzona, Switzerland 178 Mycol Progress (2008) 7:177–219 Introduction brevicompactum-type group produced harzianum A, not trichodermin. This culture was separated from the type Visible phenotype, including microscopic and colony group in a parsimony tree, but with only modest bootstrap characters, has come to occupy a role subsidiary to support (69%) (Kraus et al. 2004). molecular phylogenetics in Trichoderma and its Nielsen et al. (2005) demonstrated the production of corresponding teleomorph, Hypocrea. For example, T. alamethicins in extracts of T. brevicompactum. Alamethi- viride is the most commonly reported species in the genus, cins are a group of 20-residue polypeptides belonging to the but many, or most, of those reports are likely to have been so-called peptaibiotics. Almost 850 individual sequences of based on misidentifications because it is now known that T. linear and 9 of cyclic peptaibiotics are reported to be viride has a limited distribution in the northern hemisphere produced by members of approximately 20 fungal genera. while the morphologically very similar T. viridescens is Peptaibiotics are defined as linear or cyclic polypeptide widely distributed at temperate latitudes (Jaklitsch et al. antibiotics which (1) have a molecular weight between 500 2006). Similarly, T. harzianum also ranks among the most and 2,200 Dalton, thus containing 4–21 residues; (2) show commonly reported species, on the basis of its morphology, a high content of α-aminoisobutyric acid (Aib); (3) are but gradually this morphological concept is being refined. characterized by the presence of other non-proteinogenic Thus, the cause of green mould disease of commercial amino acids such as isovaline (Iva) and/or lipoamino acids; mushrooms was originally identified as T. harzianum but is (4) possess an acylated N-terminus, and (5), in the case of now known to be T. aggressivum (Samuels et al. 2002). the linear compounds, have a C-terminal residue that in While the physical differences between T. viride and T. most of them consists of a free or acetylated amide-bonded viridescens and between T. harzianum and T. aggressivum 1,2-amino alcohol, but might also be an amine, amide, free are small but consistent, it was only through phylogenetic amino acid, 2,5-dioxopiperazine, or sugar alcohol. The analysis that the respective pairs were seen to represent majority of linear Aib-containing peptides carries a C- distinct species. terminal residue representing a 2-amino alcohol, and this Trichoderma brevicompactum could be mistaken for T. subgroup is therefore referred to as peptaibols. Notably, half harzianum on the basis of considerable shared micro- of the known peptaibiotics are produced by strains and morphology, but phylogenetic analysis shows them to be species of the genus Hypocrea/Trichoderma (Degenkolb et only distantly related (Kraus et al. 2004). Moreover, when it al. 2003, 2006a, 2007, 2008a, b; Krause et al. 2006). was originally described (Kraus et al. 2004), a combined Peptaibiotics were proposed to contribute to the disruption ITS-tef1 phylogram indicated two, highly supported, sister of the cell walls of fungal pathogens owing to their groups within T. brevicompactum. The two well-supported amphiphilicity and membrane activity (Lorito et al. 1996). sister clades at least indicated distinct phylogenetic if not Gräfenhan (2006, see also Degenkolb et al. 2006a) reported taxonomic species. that cultures of T. brevicompactum had unusually high In their study of mycotoxin production in Trichoderma, antagonistic activity against the causal agents of two Nielsen et al. (2005) found that the ex-type and other grapevine diseases, Eutypa dieback (Eutypa lata) and Esca cultures of T. brevicompactum produced the simple tricho- disease (Phaeomoniella chlamydospora, Phaeoacremonium thecene-type mycotoxin trichodermin, while isolates in the aleophilum) when compared to other Trichoderma species sister lineage to the ex-type produced harziaum A. so far used in biological control (T. atroviride, T. Trichodermin is the first trichothecene for which the harzianum, T. koningii, and T.viride). In an effort to structure was fully elucidated; it was produced by a culture understand the in vitro antagonistic activity against the identified as T. viride LEO ND 8 (Godtfredsen and grape pathogens and, at the same time, to explore for any Vangedal 1964, 1965). That culture was reidentified by link between production of peptaibiotics and phylogeny Nielsen et al. (2005)asT. brevicompactum. Harzianum A within what they termed ‘the T. brevicompactum complex,’ was isolated from a culture identified as T. harzianum Degenkolb et al. (2006a) documented the production of (ATCC 90237, Corley et al. 1994) and later reidentified by peptaibiotics in T. brevicompactum. They also showed that Nielsen et al. (2005)asT. brevicompactum, although in the the alamethicin F30 patent strain NRRL 3199, originally sister lineage mentioned above. Because the patterns of identified as T. viride (Coats et al. 1974; Brückner and Jung toxin production by isolates coincided with the phyloge- 1980; Kirschbaum et al. 2003;Psureketal.2006), netic lineages observed in the protologue of T. brevicom- belonged to the sister clade of the ex-type strain of T. pactum, Nielsen et al. (2005) suggested the existence of brevicompactum. Degenkolb et al. (2006a) found that in two phylogenetic species within the morphological species general the patterns of peptaibiotics produced in Tricho- T. brevicompactum. However, the trichothecene results derma/Hypocrea are species-specific. The isolates in the were ambiguous in that one of the cultures (CBS 112445) type-group of T. brevicompactum did not produce tricho- identified by Kraus et al. (2004) as being in the T. brevins while those belonging to its sister clade, including Mycol Progress (2008) 7:177–219 179 NRRL 3199, did. Like other members of this clade, NRRL conidia were taken from CMD or SNA (synthetic low 3199 produced harzianum A. The peptaibiotics of CBS nutrient agar; Nirenberg 1976) within approximately 7 112445, which was weakly linked to the type group of T. days, mostly using intermittent light (12 h cool white brevicompactum (Kraus et al. 2004), were more comparable fluorescent lamps, 12 h darkness). Presence of chlamydo- to those of the type group than to those of the sister group. spores was determined by examining the underside of Since the appearance of the publications cited above, we colonies after 7–10 days on CMD with the 40× objective. have found additional cultures of the morphological species Where possible, 30 units of each character were measured, T.