Alternative reproductive strategies of Hypocrea orientalis and genetically close but clonal Trichoderma longibrachiatum, both capable of causing invasive mycoses of humans

Abstract

The common soil fungus Trichoderma (teleomorph Hypocrea, Ascomycota) shows increasing medical importance as an opportunistic human pathogen, particularly in immunocompromised and immunosuppressed patients. Regardless of the disease type and the therapy used, the prognosis for Trichoderma infection is usually poor. Trichoderma longibrachiatum has been identified as the causal agent in the majority of reported Trichoderma mycoses. As T. longibrachiatum is very common in environmental samples from all over the world, the relationship between its clinical and wild strains remains unclear. Here we performed a multilocus (ITS1 and 2, tef1, cal1 and chit18-5) phylogenetic analysis of all available clinical isolates (15) and 36 wild-type strains of the fungus including several cultures of its putative teleomorph Hypocrea orientalis. The concordance of gene genealogies recognized T. longibrachiatum and H. orientalis to be different phylogenetic species, which are reproductively isolated from each other. The majority of clinical strains (12) were attributed to T. longibrachiatum but three isolates belonged to H. orientalis, which broadens the phylogenetic span of human opportunists in the genus. Despite their genetic isolation, T. longibrachiatum and H. orientalis were shown to be cosmopolitan sympatric species with no bias towards certain geographical locations. The analysis of haplotype association, incongruence of tree topologies and the split decomposition method supported the conclusion that H. orientalis is sexually recombining whereas strict clonality prevails in T. longibrachiatum. This is a rare case of occurrence of sexual reproduction in opportunistic pathogenic fungi. The discovery of the different reproduction strategies in these two closely related species is medically relevant because it is likely that they would also differ in virulence and/or drug resistance. Genetic identity of environmental and clinical isolates of T. longibrachiatum and H. orientalis suggests the danger of nosocomial infections by Hypocrea/Trichoderma and highlights the need for ecological studies of spore dispersal as source of invasive human mycoses. INTRODUCTIONMany mould species are capable of causing invasive mycoses of mammals, including humans, under appropriate conditions, but of the more than one million fungal species which are estimated to exist in nature, only a few hundred have been associated with human and animal diseases (Walsh & Groll, 1999). 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) Myoken et al. 2002). While Trichoderma isolates are still not a major threat, they nevertheless pose difficult diagnostic and therapeutic challeng...

Phylogeny of the Clinically Relevant Species of the Emerging Fungus Trichoderma and Their Antifungal Susceptibilities

“…Nevertheless, those authors' conclusions might have been biased, since in that study only six clinical isolates were included. More recently, several studies have emphasized the importance of this species as the causal agent of human infections (4,26,27). Three other species within the clade have been associated with human disease, i.e., T. citrinoviride, T. orientale, and T. reesei (21,27,40) The latter species has not been identified in this study, but the new species T. bissettii might be considered an opportunistic human pathogen of the Longibrachiatum clade.…”

“…Other diseases attributed to members of this genus are allergic and acute invasive sinusitis (10,11), keratitis (12), otitis externa (13), skin and subcutaneous infections (14), peritonitis (9,(15)(16)(17)(18)(19)(20), deep pulmonary infections (21)(22)(23), endocarditis (24), and brain abscess (25). Most infections are caused by Trichoderma longibrachiatum, which is recognized as the main human pathogen of the genus (4,11,26), but eight other species (i.e., T. atroviride, T. citrinoviride, T. harzianum, T. koningii, T. orientale, T. pseudokoningii, T. reesei, and T. viride) have also been reported occasionally (4,(26)(27)(28). On the other hand, data on animal infections by Trichoderma spp.…”

Novel Endophytic Trichoderma spp. Isolated from Healthy Coffea arabica Roots are Capable of Controlling Coffee Tracheomycosis

“…Internal transcribed spacer region (ITS1 and 2) of the rRNA gene cluster was amplified using the primers SR6R and LR1 [21] as described by Kullnig-Gradinger et al [22]. Additionally, the amplification of approximately1.4 kb fragment of translation elongation factor 1-alpha (tef1) using primers EF1728F [23] and TEF1LLErev (5′-AAC TTG CAG GCA ATG TGG-3′) was performed as described previously (see e.g., [24]). Template DNA was purified with the QIAquick PCR Purification Kit (Qiagen, Hilden, Germany) and was subjected to automatic sequencing at Eurofins MWG Operon (Ebersberg, Germany).…”

New isolates of Trichoderma antagonistic to Sclerotinia sclerotiorum

“…GU198318.1 T. asperellum Samuels et al (2010) EU330949.1 T. brevicompactum Degenkolb et al (2008) AY857253.1 T. harzianum DQ313142.1 T. koningiopsis Samuels et al (2006) EU401576.1 T. longibrachiatum Druzhinina et al (2008) AY857246.1 T. spirale …”