Abstract
Fungal evolutionary biology is impeded by the scarcity of fossils, irregular life cycles, immortality, and frequent asexual reproduction. Simple and diminutive bodies of fungi develop inside a substrate and have exceptional metabolic and ecological plasticity, which hinders species delimitation. However, the unique fungal traits can shed light on evolutionary forces that shape the environmental adaptations of these taxa. Higher filamentous fungi that disperse through aerial spores produce amphiphilic and highly surface-active proteins called hydrophobins (HFBs), which coat spores and mediate environmental interactions. We exploited a library of HFB-deficient mutants for two cryptic species of mycoparasitic and saprotrophic fungi from the genus Trichoderma (Hypocreales) and estimated fungal development, reproductive potential, and stress resistance. HFB4 and HFB10 were found to be relevant for Trichoderma fitness because they could impact the spore-mediated dispersal processes and control other fitness traits. An analysis in silico revealed purifying selection for all cases except for HFB4 from T. harzianum, which evolved under strong positive selection pressure. Interestingly, the deletion of the hfb4 gene in T. harzianum considerably increased its fitness-related traits. Conversely, the deletion of hfb4 in T. guizhouense led to the characteristic phenotypes associated with relatively low fitness. The net contribution of the hfb4 gene to fitness was found to result from evolutionary tradeoffs between individual traits. Our analysis of HFB-dependent fitness traits has provided an evolutionary snapshot of the selective pressures and speciation process in closely related fungal species.
Highlights
Spread on land and ocean, fungi form one of the most diverse eukaryotic kingdoms with millions of species [1, 2]
To reveal HFBs that are associated with the sporulation of T. harzianum CBS 226.95 (Th) and T. guizhouense NJAU 4742 (Tg), we tested the expression of respective genes during the three stages of fungal development (Fig. 1a): (i) active growth shortly after germination when the mycelium is still developing in the substrate and no spores have formed (48 h), (ii) the formation of buoyant aerial mycelium shortly before conidiation (72 h), and (iii) mature conidiation during the climax of the life cycle (120 h) (Fig. 1b)
The results showed that two genes were highly expressed during the formation of aerial mycelium and remained highly active during conidiation: ThPTB58174 /
Summary
Spread on land and ocean, fungi form one of the most diverse eukaryotic kingdoms with millions of species [1, 2]. Previous work indicates that HFBs are secreted in a soluble form and spontaneously localize and self-organize at hydrophilichydrophobic interfaces, where they assemble into insoluble, amphipathic elastic layers [17, 18] These layers cover fungal bodies and spores in water-repelling coats [17, 19] and influence spore dispersal [20], stress resistance, development, and biotic interactions [21, 22]. In pathogenic fungi such as Aspergillus fumigatus (Eurotiales) [15], Magnaporthe grisea (Magnaporthales) [23], and Cladosporium fulvum (Capnodiales) [20], HFBs are considered as virulence factors because they reduce exposure of pathogen-associated molecular patterns (PAMPs) and antigens to receptors of the immune system. We tested the hypothesis that the HFBrelated traits are essential factors for fungal fitness, and the analysis of such traits in closely related and cryptic Trichoderma species may reveal evolutionary forces that drive fungal speciation
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