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-Zelazowska1
1 Research Area of Gene Technology and Applied Biochemistry, Institute of Chemical Engineering, Vienna University of Technology, Getreidemarkt 9/1665, A-1060 Vienna, Austria
2 Department of Microbiology, Faculty of Science and Informatics, University of Szeged, Közép fasor 52, H-6726 Szeged, Hungary
Correspondence
Irina S. Druzhinina
druzhini{at}mail.zserv.tuwien.ac.at
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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). In the last decade, however, case reports on infections by common mould fungi have increased, due to HIV/AIDS and the use of immunosuppressants for organ transplantation and cancer therapies. Species from the fungal genus Hypocrea/Trichoderma (Hypocreales, Ascomycota) have recently also joined this emerging list of such opportunistic pathogens. Detailed case reports of Trichoderma infections have been summarized by Kredics et al. (2003). Typically, these include several isolations from the peritoneal effluent of dialysis patients, infections of immunocompromised transplant recipients, and patients suffering from leukaemia, brain abscesses and HIV (Furukawa et al., 1998; Hennequin et al. 2000; Munoz et al. 1997; Myoken et al. 2002). While Trichoderma isolates are still not a major threat, they nevertheless pose difficult diagnostic and therapeutic challenges because (i) without rapid diagnosis and treatment their clinical manifestations can be fatal (Seguin et al., 1995; Tanis et al., 1995; Richter et al., 1999; Chouaki et al., 2002; Myoken et al., 2002; Tang et al., 2003), (ii) they are difficult to identify by morphological analysis (Druzhinina et al., 2005), and (iii) they are resistant to most antifungal agents (Kratzer et al., 2006).
The sources of human and animal infections by Trichoderma species, which typically are cosmopolitan soil-borne fungi frequently found in the rhizosphere or as endophytes (Klein & Eveleigh 1998; Harman et al., 2004), are not known at present. Sequence analysis of the internal transcribed spacers 1 and 2 (ITS1 and 2) of the rRNA gene cluster identified all strains isolated from clinical patients – with a few exceptions – as Trichoderma longibrachiatum (Kuhls et al., 1999; Kredics et al., 2003). This taxon usually represents a common, albeit minor, component of Trichoderma communities isolated from soil and other environments (Druzhinina et al., 2005; Kubicek et al., 2003; Kullnig et al., 2000; Wuczkowski et al., 2003; Zhang et al., 2005,), but it appears to be more abundant in indoor environments such as water-damaged buildings or mushroom farms infected by green mould disease (Thrane et al., 2001; Hatvani et al., 2007, respectively). Consequently, T. longibrachiatum has also been detected in sputum and sinus ethmoidalis of healthy humans (Kredics et al., 2003).
Many facultative pathogenic fungi such as Trichophyton rubrum, Cryptococcus neoformans and the pathogenic chytrid Batrachochytrium dendrobatidis have been shown to be single worldwide distributed clonal lineages (Gräser et al., 1999; Halliday & Carter, 2003; Morehouse et al., 2003, Zhang et al., 2006). However, some other opportunistic human pathogenic fungi such as Aspergillus fumigatus exhibit both clonal and recombining history (Nielsen & Heitman, 2007; Pringle et al., 2005). The reproduction strategy and population structure of T. longibrachiatum has not been investigated yet. Phylogenetic analyses of Trichoderma section Longibrachiatum has been limited to the sequence of the ITS regions of the rRNA genes (Kuhls et al., 1997) and RAPD (random amplified polymorphic DNA) fingerprinting (Turner et al., 1997), which both yielded results suggesting clonality for T. longibrachiatum. However, as the ascomycete Hypocrea orientalis has been proposed as a teleomorph of T. longibrachiatum (Samuels et al., 1998), at least some generations of sexual reproduction should thus be detectable in its population history.
Knowledge of the population structures of T. longibrachiatum and H. orientalis, their relationship and mode(s) of reproduction would therefore aid our understanding of whether clinical infections are caused by certain lineages only (i.e. whether they share the same recent ancestry), and whether the causative agents are present in all or only some geographical areas. The objectives of this study were therefore to (i) investigate the phylogenetic relatedness of a geographically broad sample of T. longibrachiatum and H. orientalis including clinical and environmental strains; (ii) to detect the genetic origins of clinical isolates; and (iii) to identify the mode of reproduction of these fungi with special emphasis on that of the clinical isolates.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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. The isolates are stored at –80 °C in 50 % glycerol in the laboratory of Vienna University of Technology (TU Wien). Strains are grouped according to their identification in the present work. For convenience, TU Wien collection codes (C.P.K.) are used for the strains throughout the work, but other collection numbers are also listed in Table 1.
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-Zelazowska et al., 2007). The fourth large intron of tef1 (translation elongation factor 1-
) was amplified using primers EF1-728F (5'-CATCGAGAAGTTCGAGAAGG-3') and TEF1-LLErev (5'-AACTTGCAGGCAATGTGG-3') (Jaklitsch et al., 2006), and a fragment of cal1 (calmodulin) using primers CAL-228F (5'-GAGTTCAAGGAGGCCTTCTCCC-3') and CAL-737R (5'-CATCTTTCTGGCCATCATGG-3') (Chaverri et al., 2003). Purified PCR products for ITS1 and 2, tef1, cal1 and chit18-5 were subjected to automatic sequencing at MWG (Martinsried, Germany). NCBI GenBank accession numbers of the corresponding sequences are given in Table 1
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Sequence analysis.
DNA sequences were aligned with CLUSTAL X 1.81 (Thompson et al., 1997) and then visually edited using GeneDoc 2.6 (Nicholas & Nicholas, 1997). The possibility of intragenic recombination, which would prohibit the use of the respective loci for phylogenetic analysis, was tested by linkage-disequilibrium-based statistics as implemented in DnaSP 4.50.3 (Rozas et al., 2003). The neutral evolution of coding sequences (cal1 and chi18-5) was tested by Tajima test implemented in the same software. The interleaved NEXUS file was formatted using PAUP*4.0b10 (Swofford, 2002) and manually formatted for the MrBayes v3.2 program (Ronquist & Huelsenbeck, 2003). The best nucleotide substitution model for each locus was determined using jMODELTEST (Posada, 2008). As Akaike and Bayesian information criteria [AIC (Akaike, 1974) and BIC (Schwarz, 1978), respectively] selected different nucleotide substitution models for every locus and due to the relatively small size of individual datasets (731 characters per 51 sequences for the biggest) the unconstrained GTR+I+G substitution model was applied to all sequence fragments (Table 2). Metropolis-coupled Markov chain Monte Carlo (MCMC) sampling was performed with two simultaneous runs of four incrementally heated chains that performed either 1 or 3 million generations. The length of run (number of generations) for each dataset was determined using the AWTY graphical system (Wilgenbusch et al., 2004, online at http://ceb.csit.fsu.edu/awty) to check the convergence of MCMC; all analyses were repeated at least twice. Bayesian posterior probabilities (PP) were obtained from the 50 % majority rule consensus of trees sampled every 100 generations after removing the first trees using the ‘burn’ command. The number of ‘burned’ generations was determined for every run based on visual analysis of the plot showing generation versus the log probability of observing the data. According to the protocol of Leache & Reeder (2002) PP values lower than 0.95 were not considered significant while values below 0.9 are not shown on the resulting phylograms. Model parameter summaries after MCMC runs and burning first samplings as well as nucleotide characteristics of the loci used are collected in Table 2.
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), and which was computed by using the linkage disequilibrium (LD) analysis available on the MLST website (http://linux.mlst.net/link_dis/index.htm); significance was gauged from 1000 random permutations of the data. (b) The partition homogeneity test (PHT) integrated in PAUP*4.0b10 (Swofford, 2002), which estimates the congruence among different loci datasets (Cunningham, 1997). For this test heuristic search under the parsimony optimality criterion was used, parsimony-uninformative characters were excluded, gaps were treated as missing, and 10 000 repetitions were performed. A maximum of 100 trees were saved to conserve memory. (c) Recombination tests implemented in the RecombiTEST package available at http://www.lifesci.sussex.ac.uk/CSE/test/. (d) The 
w test (pairwise homoplasy index, Phi) as implemented in the SplitsTree software (Huson, 1998). (e) Visual analysis of topologies of phylogenetic trees. |
RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; online at http://www.ISTH.info). Among these strains, 15 were obtained as clinical isolates. The other 36 were chosen to cover the broadest possible geographical variability of T. longibrachiatum including all available strains (7) of its putative teleomorph H. orientalis. In order to investigate the evolutionary relations within this sample, we sequenced three phylogenetic markers used in Hypocrea/Trichoderma: the long intron of tef1, an intron-containing fragment of cal1 and a partial exon sequence of chi18-5. Nucleotide characteristics of these sequences are given in Table 2.
We used Bayesian analysis of the individual gene datasets to infer a phylogenetic structure (Fig. 1a–c). Three statistically supported clades and a single lone branch were present in the tef1 and chi18-5 gene trees (Fig. 1a, b): the PS (phylogenetic species) I clade contained more than half the isolates, including the ex-type strain of T. longibrachiatum; clade PS II included the ex-type strain of H. orientalis, all but one (C.P.K. 1261) of the other strains of H. orientalis, and three strains originally identified as T. longibrachiatum; clade PS III contained three strains isolated from coffee rhizosphere in Ethiopia. The single strain isolated from the teleomorph from New Zealand (C.P.K. 1261) formed a branch with unresolved phylogenetic position within the dataset studied. Resolution of the cal1 tree (Fig. 1c) was less clear as no statistical support was detected for clade PS I, but its topology was in agreement with the other two loci. The phylogenetic position of strains forming clade PS II in tef1 and chi18-5 trees was not well resolved by cal1 analysis as C.P.K. 2880 and C.P.K. 2881 formed a topologically separated subclade (but without statistical support) from other strains of PS II. Positions of C.P.K. 1261 and PS III on the cal1 tree were concordant with the other two loci.
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for multilocus genealogies – i.e. that a clade must be present in the majority of single-locus trees; and that a clade is reliably supported by at least one single-locus genealogy and is not contradicted by any other single-gene tree determined by the same methods (the genealogical nondiscordance criterion). Based on the position of the ex-type strains for T. longibrachiatum and H. orientalis in different clades, we conclude that clade PS I represents T. longibrachiatum sensu stricto, and clade PS II consequently represents H. orientalis. On the other hand, clade PS III and C.P.K. 1261 are two as yet undescribed species of section Longibrachiatum which we will further refer to as Trichoderma sp. PS (phylogenetic species) III and Hypocrea sp. PS IV, respectively.
The clinical strains of ‘T. longibrachiatum’ were only found in clades PS I (12 strains) and II (3 strains) and thus – in contrast to what was believed before – belong to two phylogenetic species (Fig. 1).
Reproductive strategies of T. longibrachiatum and H. orientalis
In order to test whether the phylogenetically distinct species T. longibrachiatum and H. orientalis are also separated by a reproductive barrier, we used the split decomposition method provided by the SplitsTree (Huson & Bryant, 2006) package. This analysis enabled us to test for the presence of network relationships within clades PS I, II and III, and various dual and threefold combinations of them, using a concatenated dataset of tef1, cal1 and chit18-5 (Fig. 2a–c). This method presents conflicting phylogenetic data, presumably arising from recombination, as an interconnected network of lineages. As shown in Fig. 2(a), such a network was evident between the total dataset (four phylogenetic species). However, analyses of individual clades PS I and PS II documented an almost complete lack of a network for T. longibrachiatum compared to H. orientalis, which is expected to have sexual reproduction in its life cycle as several teleomorphs were collected. When the Phi test (Huson & Bryant, 2006) implemented in the same software package was applied to various concatenated gene combinations of clades PS I, PS II and PS III, evidence for recombination was obtained for every combination (data not shown) and also for clade PS II (H. orientalis) alone (=0.32, P=0.0005), whereas the possibility of recombination was rejected for clade PS I (T. longibrachiatum) (=0.14, P=0.58). These data indicate that in contrast to H. orientalis, which represents a sexual population, T. longibrachiatum is largely clonal. Strains of PS III could not be analysed individually because they were too low in number.
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) was used to examine the congruence between gene trees. In this test artificial datasets are produced by multiple (10 000) resampling and random swapping of observed datasets and subsequent construction of maximum-parsimony trees for every newly sampled ‘gene’ sequence. For clonally reproducing populations, the sums of the lengths of the gene trees for the observed and resampled data should be similar, but under recombination the sums of the tree lengths should be longer than that for the actual data because recombination among unlinked sites should introduce homoplasy into the data. When the whole dataset was analysed (PS I–IV; cal1, chi18-5 and tef1) the actual summed tree length of 189 steps was exactly at the lowest limit of that produced by any of the 10 000 artificial datasets (P=0.0003), and eight steps shorter than 0.95 % of them, thus indicating incongruence among the different gene trees. In order to test whether this topological conflict appears to be due to incongruence in one particular clade the PHT was applied to the PS I and PS II clades separately. In addition, we ran the analysis with and without partition of the tef1 gene, which covers the intron sequence and therefore may contain homoplasious characters even in clonal populations, due to high mutation rates. The corresponding data show (Fig. 3) that there is a recombination within the PS II H. orientalis clade, the result being independent of tef1 sequences. At the same time, topologies of cal1 and chi18-5 trees for PS I T. longibrachiatum are congruent, suggesting the absence of sexual recombination in this clade (Fig. 3). When tef1 was included in the PHT of PS I the null hypothesis of recombination was not rejected (P=0.046).
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). The data obtained were in accordance with occurrence of recombination within H. orientalis but not in T. longibrachiatum and Trichoderma sp. PS III, as the IA test did not reject the null hypothesis of recombination in the former (P=0.462) but did so in the latter two datasets.
Finally, the maximum chi-squared test of Maynard Smith (1992), linkage disequilibrium (LD) r2 (Hill & Robertson, 1968), and LDD' (LD versus distance |D|; Lewontin, 1964) estimates available on the RecombiTEST webpage (see Methods) also detected recombination between strains of H. orientalis, but not in T. longibrachiatum (data not shown).
Inspection of intracladal structures of H. orientalis on all trees revealed several conflicts of topologies. Besides the abovementioned unresolved position of C.P.K. 2880 and C.P.K. 2881 on the cal1 tree, other strains of PS II aggregated in different statistically supported subclades which were unique for every locus. Such ‘jumping’ behaviour of individual sequences also suggests the presence of sexual recombination. No intracladal patterns were detected for PS I and III.
Haplotype structure and distribution of clinical strains within the T. longibrachiatum clade
Since the above data showed that T. longibrachiatum behaves essentially clonally, we now tested whether the clinical isolates would occupy specific positions in the structure of clade PS I, i.e. whether clinical occurrence would correlate with specific haplotypes. To this end, we used DnaSP 4.50.3 to collapse individual sequence alignments to haplotypes, and then subjected them to statistical parsimony implemented in TCS (Clement et al., 2000). The results showed that the haplotype with the highest total numbers of environmental isolates also contained the majority of clinical isolates. Haplotypes represented by only a single strain contained only a few individual clinical isolates, but most of them were represented by wild-type strains (data not shown).
Biogeography of T. longibrachiatum and H. orientalis
The distribution analysis of strains from PS I and II shows that T. longibrachiatum and H. orientalis are a closely related pair of cosmopolitan and sympatric species, as both of them were detected on almost all continents. H. orientalis was frequently isolated from soil or mud samples as the anamorph, so it is clearly a holomorphic species which may coexist with T. longibrachiatum in the same ecosystem. The only known teleomorph samples of H. orientalis have so far been collected in China, thus making it difficult to speculate on climatic preferences for fruit body formation. Unfortunately the origin of several clinical isolates (6; Table 1) was not available for this study. The other strains were isolated from hospitals in North America (south United States and north-east Canada), temperate Europe (central France and Austria), subtropical Gran Canaria and continental Spain. This dataset shows that there is no bias of clinical strains towards specific geographical location.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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) and study of mitochondrial DNA polymorphism (Antal et al., 2006). We have thus demonstrated that both species are a potential threat. It is important to mention that human clinical isolates shared identical multilocus haplotypes with isolates from soil and plant materials, and Trichoderma invasive mycoses may therefore be potentially nosocomial.
The finding of this work has important implications also for the biotechnological use of T. longibrachiatum, because strains of this fungus have been used as agents of biological control against phytopathogenic fungi (Vizcaíno et al., 2005; Sánchez et al., 2007). In the light of the present results, this application should be abandoned or at least carefully monitored. Also, T. longibrachiatum has been reported to be a component of the indoor fungal flora (Thrane et al., 2001) and has also frequently been isolated from mushroom farms infected by green mould disease (Hatvani et al., 2007). We recommend that T. longibrachiatum and H. orientalis are included on the list of those indoor fungi whose presence is specifically monitored. Primers to be designed for such tests therefore have to take into account the whole genetic variation within T. longibrachiatum and H. orientalis, as demonstrated in this paper. The lower percentage of H. orientalis clinical strains may be a result of the lower sample size. Interestingly, clinical isolates in the H. orientalis clade were recovered during the last 5 years, whereas isolates recovered earlier were only T. longibrachiatum.
There have so far been no studies dedicated to the ecology of T. longibrachiatum and H. orientalis. Therefore it is difficult to trace their preferred ecological niches, which would aid prediction of the source of Trichoderma infections. Nevertheless, besides being isolated from numerous soil samples worldwide, T. longibrachiatum has been consistently detected in association either with wild fruiting bodies of the wood-decaying fungus Pleurotus ostreatus (L. Hatvani, L. Kredics, I. S. Druzhinina & C. P. Kubicek, unpublished) or in mushroom farms cultivating Pleurotus and Agaricus (Hatvani et al., 2007). Another also interesting case of abundant detection of T. longibrachiatum was its isolation from the archaeological excavation sites at an Iron Age tomb in the Republic of Tatarstan, Russia (F. Alimova & I. S. Druzhinina, unpublished). An explanation for these findings may be derived from observations that T. longibrachiatum occupies the lowest soil horizons but not the upper organic soil layers. Therefore, together with its appearance as causative agent of invasive mycoses, there is emerging evidence that T. longibrachiatum and H. orientalis may have a specialized ecological niche(s) which is(are) essentially different from other species of the genus.
The present findings distinguish infections caused by T. longibrachiatum and H. orientalis from those caused by human-pathogenic fungi from the Fusarium solani complex, where the majority of clinical isolates are derived from a single worldwide distributed clonal lineage (Zhang et al., 2006). A clonal structure has also been demonstrated for other pathogenic fungi such as Trichophyton rubrum, Cryptococcus neoformans or the chytrid pathogen Batrachochytrium dendrobatidis (Gräser et al., 1999; Halliday & Carter, 2003; Morehouse et al., 2003), whereas many other human-pathogenic fungi, including Aspergillus fumigatus (Pringle et al., 2005), exhibit both clonal and recombining strategies (for reviews see Taylor et al., 1999; Nielsen & Heitman, 2007). The results from this study present evidence that sexual reproduction, indicated by recombination, is an important strategy in one of the two opportunistic pathogenic species of Hypocrea/Trichoderma, H. orientalis. The potential presence of a sexual life cycle in an opportunistic pathogen is a significant finding, because its allows the fungus to respond faster to environmental challenges, thereby combating disease treatment by exchange of antibiotic-resistance genes and virulence factors (Milgroom, 1996; Nielsen & Heitman, 2007; Normak et al., 2003; Paoletti et al., 2005). It is not known whether these two species exploit their animal-pathogenic ability in nature; therefore it is too early to speculate that H. orientalis has developed different strategies than T. longibrachiatum for its opportunistic attack and subsequent survival. The phylogenetic analysis presented in this paper suggests that T. longibrachiatum and H. orientalis evolved in parallel from a common ancestor, forming two sympatric species. Thus, their pathogenic ability would be the result of a heritage from a recent ancestor rather than a convergent evolution. Further studies are needed to understand which species exploits more of its pathogenic abilities in nature.
H. orientalis is not the only Hypocrea species with potential health risk to humans. Druzhinina et al. (2008) reported a case study in which Hypocrea sp. CBS 120951 was isolated from the lung tissue of a patient with non-fatal pulmonary fibrosis. This isolate exhibits an uncertain phylogenetic position in the genus Hypocrea/Trichoderma and is also phenotypically very distinct as it does not conidiate in vitro but produces fertile stromata. Nevertheless, cases of sexual reproduction among clinically relevant strains of Hypocrea may be more frequent than was previously recognized.
Apart from these clinical implications, the results presented here also provide some new insights into the taxonomy of T. longibrachiatum and H. orientalis: based on ITS1 sequence analysis and isoenzyme data, Samuels et al. (1998) suggested that T. longibrachiatum may be the anamorph of H. orientalis. The present data reject this hypothesis by clearly showing that these two taxa represent individual phylogenetic species, which have already undergone reproductive isolation. In addition, we provide evidence for a third phylogenetic species, Trichoderma sp. PS III, which should be formally described elsewhere. In addition, the branches leading to this species did not form a network in the split decomposition analysis although the three available strains were isolated from three different coffee-growing areas in Ethiopia. These data are supportive of a reproductive barrier between Trichoderma sp. PS III, T. longibrachiatum and H. orientalis.
Hypocrea sp. strain C.P.K. 1261 (=CBS 243.63) formed a separate branch in all gene trees and in the SplitsTree analysis. Samuels et al. (1998) had previously noted that this strain differed from the other isolates in their sample both morphologically and in isoenzyme analysis profiles but nevertheless maintained it within their concept of H. orientalis. Based on our data, this strain represents a fourth species in our dataset. Since the origin of this strain was from a fruiting body, it is a member of another sexually propagating population which could occupy an as yet unknown ecological niche.
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ACKNOWLEDGEMENTS |
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Edited by: H. A. B. Wösten
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Received 7 June 2008;
revised 14 July 2008;
accepted 21 July 2008.
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