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A New Species of Trichoderma Hypoxylon Harbours Abundant Secondary Metabolites Received: 13 May 2016 Jingzu Sun1,2, Yunfei Pei1,†, Erwei Li1, Wei Li1, Kevin D

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A New Species of Trichoderma Hypoxylon Harbours Abundant Secondary Metabolites Received: 13 May 2016 Jingzu Sun1,2, Yunfei Pei1,†, Erwei Li1, Wei Li1, Kevin D www.nature.com/scientificreports OPEN A new species of Trichoderma hypoxylon harbours abundant secondary metabolites Received: 13 May 2016 Jingzu Sun1,2, Yunfei Pei1,†, Erwei Li1, Wei Li1, Kevin D. Hyde2, Wen-Bing Yin1,3 & Accepted: 27 October 2016 Xingzhong Liu1,3 Published: 21 November 2016 Some species of Trichoderma are fungicolous on fungi and have been extensively studied and commercialized as biocontrol agents. Multigene analyses coupled with morphology, resulted in the discovery of T. hypoxylon sp. nov., which was isolated from surface of the stroma of Hypoxylon anthochroum. The new taxon produces Trichoderma- to Verticillium-like conidiophores and hyaline conidia. Phylogenetic analyses based on combined ITS, TEF1-α and RPB2 sequence data indicated that T. hypoxylon is a well-distinguished species with strong bootstrap support in the polysporum group. Chemical assessment of this species reveals a richness of secondary metabolites with trichothecenes and epipolythiodiketopiperazines as the major compounds. The fungicolous life style of T. hypoxylon and the production of abundant metabolites are indicative of the important ecological roles of this species in nature. Traditionally the taxonomy of species of Trichoderma was based on morphology. Most species in this genus are usually fast growing, produce highly branched conidiophores with cylindrical to nearly subglobose phialides and ellipsoidal to globose conidia1–4. However, high morphological homoplasy in sexual state makes identification difficult, and the importance of sequence data have been increased5,6. Based on the combined phenotypic and phylogenetic analysis, about 260 species have been recognized and accepted5–10. The internal transcript spacers (ITS), translation elongation factor 1-alpha (TEF1-α) and largest subunit of RNA polymerase II (RBP2) genes are more available to recognize species within Trichoderma5,9,10. Phylogenetic analysis based on a combination of ITS, TEF1-α and RBP2 are recommended solve the problem of Trichoderma species complex and reveal taxonomic deversity2,6–11. Fungi associated with other fungi as saprobes, commensals or parasites are termed fungicolous fungi12. These fungi usually produce rich secondary metabolites, which have been reported as an important resource for bio- active small molecule discovery such as anti-fungi, tumors, nematodes and bacteria13,14. Some metabolites pro- duced by the species in this genus play very important ecological roles in nature15. Trichoderma species are most frequently found in vegetable matter, decaying wood and soil, plant rhizosphere, as well as on other fungi5,6,16. Fungicolous Trichoderma species comprise diversity and abundant genes associated with secondary metabolites productivity15,16. These genes are responsible to a number of secondary metabolites with pharmaceutical and biotechnological importance including peptides, peptaibols, poliketides, pyrones, siderophores and nonvolatile terpenes14,15–22. Some of secondary metabolites are responsible for survival and adaption of their habitat15,16. For example, peptaibols are small peptides of non-ribosomal origin produced by Trichoderma15 and have the ability to induce systemic resistance in plants against microbial invasion. Harzianum A is a growth-promoting trichoth- ecene produced by Trichoderma arundinaceum17. In the search of novel bioactive compounds, we carried out resource and diversity investigation of fungicolous fungi in China and Thailand. Two isolates of Trichoderma were obtained from stroma of Hypoxylon anthochroum. They are described, illustrated and named as a new species Trichoderma hypoxylon. Its phylogenetic positions 1State Key Laboratory of Mycology, Institute of Microbiology, Chinese Academy of Sciences (CASIM), No. 3 Park 1, West Beichen Road, Chaoyang District, Beijing 100101, China. 2Center of Excellence in Fungal Research, and School of Science, Mae Fah Luang University, Chiang Rai, 57100, Thailand. 3Joint Laboratory of Applied Microbial Technology, CASIM and Institute of Biology limited Liability Company, Henan Academy of Sciences, Zheng Zhou, 45002, China. †Present address: National Institutes for Food and Drug Control, No. 2, Tiantan Xili, Dongcheng District, Beijing 100050, China. Correspondence and requests for materials should be addressed to W.-B.Y. (email: [email protected]) or X.L. (email: [email protected]) SCIENTIFIC REPORTS | 6:37369 | DOI: 10.1038/srep37369 1 www.nature.com/scientificreports/ Figure 1. Phylogeny constructed from the combined sequences of ITS, TEF1-α and RBP2. The tree is rooted to Nectria berolinensis and Nectria eustromatica. MPBP above 50% (left) MLBP above 50% (midle) BIPP above 95% (right) are indicated at the nodes. New species proposed are indicated in boldface. were also explored, which inferred from sequence analyses of the combined internal transcribed spacer (ITS), partial RNA polymerase II subunit (RPB2) and translation elongation factor 1 alpha (TEF1-α ) exon genes. Detailed comparisons were made between the new taxa and their related fungi. Considering T. hypoxylon is a new fungicolous species and its special life style, we reasoned that it is valued to study the chemical profiles to get the linkage to the biological roles. Results Phylogenetic analyses. Alignment results show that the sequences ITS, RPB2 and TEF1-α of T. hypoxy- lon are less than 97% similar to other Trichoderma species. Based on phylogenetic analysis of single gene of ITS, RPB2 and TEF1-α , T. hypoxylon formed a clade with Trichoderma taxi and Trichoderma rubi. The position of this clade showed closed relationship with section Hypoceanum, Polysporum, Psychrophila and other species in Trichoderma (Fig. S1, and Fig. S2). The phylogenetic analysis of RPB2 showed that T. hypoxylon grouped with the Polysporum section (Fig. S3). Therefore, the combination matrix included 60 ingroup taxa of Trichoderma which are phylogenetically close to T. hypoxylon. This data matrix comprised 2839 characters. Bayesian inference (BI), maximum likelihood (ML) and maximum parsimony (MP) trees generated shared the same topology. In MP analyses, 1642 (57.8%) characters are constant, 216 (7.6%) characters are parsimony-uninformative, and 981 (34.6%) characters are parsimony informative. In MP analyses, 1642 characters were constant, 981 were parsi- mony-informative, and 216 variable characters were parsimony-uninformative. Maximum likelihood tree was Presented (Fig. 1). Based on the analyses, 60 strains of Trichoderma, including our new species T. hypoxylon, formed a strongly supported group (MPBP/MLBP/BIPP =​ 100%/100%/1.00). They also clustered in 7 recog- nized subclades and a new subclade including T. hypoxylon, Brevicompactum (MLBP/BIPP = 94%/1.00), Deliquescens (MPBP/BIPP =​ 100%/1.00), Hypoceanum (MPBP/MLBP/BIPP = 100%/99%/1.00), Polysporum (BIPP =​ 1.00), Psychrophila (MPBP/MLBP/BIPP =​ 98%/96%/1.00), and green spore sections (MPBP/MLBP/ BIPP =​ 100%/100%/1.00), whereas two strain of Trichoderma atroviride Bissett positioned inside Polysporum section. The tree topology is basically congruent with previous reports6. SCIENTIFIC REPORTS | 6:37369 | DOI: 10.1038/srep37369 2 www.nature.com/scientificreports/ Figure 2. Morphologicial characteristics of Trichoderma hypoxylon (ex-type CGMCC 3.17906) on PDA. (a–c) and (h–k) conidiophores with condia; (d–g) conidiophores without condia; l, conidia; bar = 10 μ m. The new species T. hypoxylon (CGMCC 3.17906, CGMCC 3.17907), and T. taxi and T. rubi formed a clade independent from other Trichoderma species with strong support (MPBP/MLBP/BIPP = 100%/100%/1.00). However, T. hypoxylon isolates were distinguished from T. axi and T. rubi with high support (MPBP/MLBP/ BIPP = 100%/100%/1.00). SCIENTIFIC REPORTS | 6:37369 | DOI: 10.1038/srep37369 3 www.nature.com/scientificreports/ Figure 3. Morphologicial characters of Trichoderma hypoxylon (ex-type CGMCC 3.17906) on CMD after 30 days. (a) Forward of the colony; (b) reverse of the colony; (c) mycelia; (d,e,i) conidiophores with condia; (h) conidiophores without condia; (j) conidia; c = 1000 μ m; (d) e = 20 μ m; c f–j = 10 μ m. SCIENTIFIC REPORTS | 6:37369 | DOI: 10.1038/srep37369 4 www.nature.com/scientificreports/ Figure 4. Cultures of Trichoderma hypoxylon on PDA, CMD and SNA at different temperature after 10 days. (a–c) Colony on PDA at 30 °C, 25 °C and 20 °C seperately; (d–f) colony on CMD at 30 °C, 25 °C and 20 °C seperately; (g–i) colony on SNA at 30 °C, 25 °C and 20 °C seperately. Taxonomy. Trichoderma hypoxylon Jing Z. Sun, Xing Z. Liu & K.D. Hyde, sp. nov. Index Fungorum number: IF552046, Facesoffungi number: FoF: 02075, Figs 2–4. Type:—HMAS 246918 Colonizing or hyperparasitic on stroma of Hypoxylon anthochroum. Sexual morph Undetermined. Asexual morph forming Acremonium- to Verticillium-like conidiophores and hyaline conidia. Phialides lageniform to cylindrical, hyaline, 4.5–12 × 3–3.5 μ m (x =​ 6.5 ±​ 1.4 × 3.2 ±​ 0.25 μ m, n =​ 30); l/w 2.5–4(− 4.5) (n = 30). Mature conidia forming a head at the apex of conidiophores, hyaline, smooth-walled, unicellular, oboviod and mostly 2.8–4.3 × 2.1–2.4 μ m (x = 3.8 ± 0.4 × 2.2 ± 0.10 μ m, n =​ 30), l/w 1–2(− 2.2) (n =​ 30). Slow growing on PDA, SNA and CMD; PDA colonies especially dense, whitish; SNA and CMA colonies consisting of concentric rings with irregular outline when cultured in darkness at 30 °C. Colonies on PDA after 10 d at 20, 25 and 30 °C dense (Fig. 4a–c), with a thick white layer of cotton-like aerial mycelia, forming concentric rings at 20 and 25 °C, however not forming concentric rings at 30 °C, odour woody, and agar not pigmented. Conidia formed within 10 d in the aerial mycelium, mature conidia gathered at the apex of conidiophores, hyaline, smooth walled, 1-celled, oboviod and mostly 2.8–4.3 × 2.1–2.4 μ m (x = 3.8 ± 0.4 × 2.2 ± 0.10 μ m, n =​ 30), l/w 1.2–2.2 (− 2.5) (n = 30). Colony on CMD after 10 d at 20, 25 and 30 °C flat (Fig. 4d–f), with a thin white layer of mycelia, not forming concentric rings and conidia at 20 and 25 °C, however forming concentric rings at 30 °C, no distinctive odour, agar not pigmented.
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