Category: Publications

Kubicek, C.P., Steindorff, A.S., Chenthamara, K., Manganiello, G., Henrissat, B., Zhang, J., Cai, F., Kopchinskiy, A.G., Kubicek, E.M., Kuo, A., Baroncelli, R., Sarrocco, S., Noronha, E.F., Vannacci, G., Shen, Q.*, Grigoriev, I.V., Druzhinina, I.S.*, 2019. Evolution and comparative genomics of the most common Trichoderma specieshttps://pubmed.ncbi.nlm.nih.gov/31189469/. BMC Genomics 20.

Background

The growing importance of the ubiquitous fungal genus Trichoderma (Hypocreales, Ascomycota) requires understanding of its biology and evolution. Many Trichoderma species are used as biofertilizers and biofungicides and T. reesei is the model organism for industrial production of cellulolytic enzymes. In addition, some highly opportunistic species devastate mushroom farms and can become pathogens of humans. A comparative analysis of the first three whole genomes revealed mycoparasitism as the innate feature of Trichoderma. However, the evolution of these traits is not yet understood.

Results

We selected 12 most commonly occurring Trichoderma species and studied the evolution of their genome sequences. Trichoderma evolved in the time of the Cretaceous-Palaeogene extinction event 66 (±15) mya, but the formation of extant sections (Longibrachiatum, Trichoderma) or clades (Harzianum/Virens) happened in Oligocene. The evolution of the Harzianum clade and section Trichoderma was accompanied by significant gene gain, but the ancestor of section Longibrachiatum experienced rapid gene loss. The highest number of genes gained encoded ankyrins, HET domain proteins and transcription factors. We also identified the Trichoderma core genome, completely curated its annotation, investigated several gene families in detail and compared the results to those of other fungi. Eighty percent of those genes for which a function could be predicted were also found in other fungi, but only 67% of those without a predictable function.

Conclusions

Our study presents a time scaled pattern of genome evolution in 12 Trichoderma species from three phylogenetically distant clades/sections and a comprehensive analysis of their genes. The data offer insights in the evolution of a mycoparasite towards a generalist.

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Ding, M., Chen, W., Gao, R., Jiang, S., Zhao, Z., Cai, F., and Druzhinina, I. S. Emerging salt marshes as a source of Trichoderma arenerea sp. nov. and other fungal bioeffectors for biosaline agriculture, Journal of Applied Microbiology, doi: 10.1111/jam.14751.

Aims: Sustainable agriculture requires effective and safe biofertilizers and biofungicides with low environmental impact. Natural ecosystems that closely resemble the conditions of biosaline agriculture may present a reservoir for fungal strains that can be used as novel bioeffectors.

Methods and results: We isolated a library of fungi from the rhizosphere of three natural halotolerant plants grown in the emerging tidal salt marshes on the southeast coast of China. DNA barcoding of 116 isolates based on the rRNA ITS1 and 2 and other markers (tef1 or rpb2) revealed 38 fungal species, including plant pathogenic (41%), saprotrophic (24%), and mycoparasitic (28%) taxa. The mycoparasitic fungi were mainly species from the hypocrealean genus Trichoderma, including at least four novel phylotypes. Two of them, representing the taxa Trichoderma arenarium sp. nov. (described here) and T. asperelloides, showed effective antagonistic activity against five phytopathogenic fungi, and significant growth promotion on tomato seedlings under the conditions of saline agriculture.

Conclusions: Trichoderma spp. of salt marshes play the role of natural biological control in young soil ecosystems with a putatively premature microbiome.

Significance and impact: The saline soil microbiome is a rich source of halotolerant bioeffectors that can be used in biosaline agriculture.

Keywords: Trichoderma arenarium; Biosaline agriculture; Halotolerant fungi; Plant growth promotion; Rhizosphere; Salt marsh.

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Cai, F., Gao, R., Zhao, Z., Ding, M., Jiang, S., Yagtu, C., Zhu, H., Zhang, J., Ebner, T., Mayrhofer-Reinhartshuber, M., Kainz, P., Chenthamara, K., Bayram-Akcapinar, G., Shen, Q., and Druzhinina, I. S. 2020 Evolutionary compromises in fungal fitness: hydrophobins hinder the adverse dispersal of spores and challenge their survival, The ISME J 14, 2610–2624 (2020). https://doi.org/10.1038/s41396-020-0709-0

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.

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Gao, R., Ding, M., Jiang, S., Zhao, Z., Chenthamara, K., Shen, Q. Cai, F., Druzhinina I.S. 2020. The evolutionary and functional paradox of cerato-platanins in the mycoparasitic fungi. Applied and Environmental Microbiology 86:e00696-20

Cerato-platanins (CPs) form a family of fungal small secreted cysteine-rich proteins (SSCPs) and are of particular interest not only because of their surface activity but also their abundant secretion by fungi. We performed an evolutionary analysis of 283 CPs from 157 fungal genomes with the focus on the environmental opportunistic plant-beneficial and mycoparasitic fungus Trichoderma Our results revealed a long evolutionary history of CPs in Dikarya fungi that have undergone several events of lateral gene transfer and gene duplication. Three genes were maintained in the core genome of Trichoderma, while some species have up to four CP-encoding genes. All Trichoderma CPs evolve under stabilizing natural selection pressure. The functional genomic analysis of CPs in Trichoderma guizhouense and Trichoderma harzianum revealed that only epl1 is active at all stages of development but that it plays a minor role in interactions with other fungi and bacteria. The deletion of this gene results in increased colonization of tomato roots by Trichoderma spp. Similarly, biochemical tests of EPL1 heterologously produced by Pichia pastoris support the claims described above. Based on the results obtained, we conclude that the function of CPs is probably linked to their surfactant properties and the ability to modify the hyphosphere of submerged mycelia and, thus, facilitate the nutritional versatility of fungi. The effector-like functions do not sufficiently describe the diversity and evolution of these proteins in fungi, as they are also maintained, duplicated, or laterally transferred in the genomes of nonherbivore fungi.

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