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Cai et al. 2020 Evolutionary compromises in fungal fitness: hydrophobins hinder the adverse dispersal of spores and challenge their survival, The ISME J

The role of HFB4 in Trichoderma fitness

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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Irina S. Druzhinina, Ph. D.

Irina S. Druzhinina

Nanjing Agricultural University, College of Resources and Environmental Sciences

Weigang NO. 1, Nanjing, P.R. China, 210095 Tel +86 15 996344211

FungiG Fungal Genomics Group

Website:             www.FungiG.org

Email:                   Irina.druzhinina@njau.edu.cn

ORCID:                   0000-0003-2821-5268

Research Gate: https://www.researchgate.net/profile/Irina-Druzhinina

Google Scholar: https://scholar.google.com/citations?user=TRnrszkAAAAJ&hl=ru&oi=ao

Professor (Full), Fungal Genomics Laboratory (FungiG), Leader

Editor, Applied and Environmental Microbiology (AEM), ASM

Associate Editor, Mycoasia

Editorial Board Member, Fungal Biology and Biotechnology, BMC

Editorial Board Member, Journal of Fungi (JoF), MDPI

Guest SI Editor, Science of the Total Environment

Head of the TU Wien Collection of Industrial Microorganisms, Vienna, Austria

Head of the International Committee of Trichoderma Taxonomy www.trichoderma.info (ICTT)

Coordinator and co-PI of the Trichoderma whole genus genomics project, JGI DOE, Berkeley, USA

Druzhinina-CV-February-2022-with-publications-1Download
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Gao et al. 2020. The evolutionary and functional paradox of cerato-platanins in the mycoparasitic fungi. Applied and Environmental Microbiology

Cerato-platanins in hyphosphere

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.

Gao et al., 2020 AEM https://pubmed.ncbi.nlm.nih.gov/32332135/

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Renwei Gao

FungiG Renwei Gao

I am a FungiG Ph.D. student interested in the genetic engineering and functional genetics of fungi. I feel fascinated by how wonderful the eukaryotic cell is. Although it is the result of evolution, it follows a particular rule as if it is arranged. My primary research is focused on the surface-active small secreted cysteine-rich proteins (saSSCPs) in Trichoderma, such as cerato-platanins and HFBs. 

My recent publications:

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

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

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.

Jiang S-Q, Yu Y-N, Gao R-W, Wang H, Zhang J, Li R, Long X-H, Shen Q-R, Chen W, Cai F: High-throughput absolute quantification sequencing reveals the effect of different fertilizer applications on bacterial community in a tomato cultivated coastal saline soil. Science of The Total Environment 2019, 687:601-609.

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Feng Cai

Feng Cai

Feng Cai, Ph.D

ORCID: 0000-0003-2032-6190

Current position: Postdoc

Tel.: +86 (0)25 84396825

E-mail: fengcai@njau.edu.cn

Address: Yifulou 5064, Weigang 1, Nanjing 210095, P.R. China

Research Gate

RESEARCH INTEREST

I am mainly working on fungal ecological genomics using Trichoderma spp. as the model for fitness, speciation, diversity, and evolution. Ubiquitously spread on land and ocean, fungi form one of the most diverse eukaryotic phyla with millions of species. However, the peculiarities of their biology such as their pleomorphic life cycles with a frequent prevalence of asexual reproduction, prolonged stages of dormancy, and superior metabolic plasticity impede studies on fungal evolution and ecology, leaving this group largely unexplored. On the other hand, the unique fungal traits can shed light on the evolutionary forces that shape their environmental adaptions. Filamentous fungi that disperse through aerial spores produce unique amphiphilic and highly surface-active proteins, hydrophobins (HFBs), which coat spores and mediate a multitude of environmental interactions. We recently exploited a library of hfb-edited mutants for closely related Trichoderma species and the HFBome in this fungus at a genus-wide level. The results pointed fungal HFBs are linked with their fitness that addresses fungal development, reproductive potential, and stress resistance. And the net contribution of such genes to fitness was found to result from the evolutionary tradeoff between individual effects. In parallel, the question of how spores get coated by such a huge HFB matrix on their surface also raised the interest of our research. Using the HFB-enriched mold Trichoderma and the HFB‐free yeast Pichia pastoris, we found that HFBs tended to accumulate in lipid bodies (LBs). Subsequent internalization of such LBs in vacuoles resulted in the maintenance of turgor pressure in aerial hyphae which are seen as “conidia rings” on colonies. Besides, I am also interested in exploring the functional roles of other small secreted cysteine-rich proteins (SSCPs) playing in the complex environment called the “hyphosphere” that is created by the fungus itself.

RESEARCH KEYWORDS

Cerato-platanin (CP), DNA barcoding, Ecological genetics, evolution, fungal-bacterial interaction, fungal-plant interaction, fungal diversity, fitness, halotolerant microbes, hydrophobin (HFB), new fungus exploration, phylogeny, plastic biodegradation, saline agriculture, small secreted cysteine-rich proteins (SSCP), spore dispersal, soil microbiome, speciation, Trichoderma, WGS

PRESENTATIONS ON THE INTERNATIONAL CONFERENCES

(Talk) “Never shall those born to crawl, learn to fly: Evolutionary compromises between spore hydrophobicity and fitness in Trichoderma”. The 15th European Conference on Fungal Genetics (ECFG15), February 2020. Rome, Italy.

(Talk) “Hydrophobins influence fungal fitness by modulating spore dispersal and survival”, Session “Fungal spore: development, dormancy, and germination”. The 30th Fungal Genetics Conference, March 2019. Asilomar, CA, USA.

(Poster) “Unconventional secretion of hydrophobins by aerial hyphae resembles the autophagy and explains the conidiation landscape of Trichoderma colony”. The 30th Fungal Genetics Conference, March 2019. Asilomar, CA, USA.

(Poster) “Hydrophobins constitute the major part of the massive extracellular matrix of the conidiating Trichoderma colony and influence its fitness by modulating spore dispersal and survival”. The 30th Fungal Genetics Conference, March 2019. Asilomar, CA, USA.

(Poster) “Hydrophobins of Trichoderma guizhouense inhibit tomato defense system for successful colonization of rhizosphere”. The 13th European Conference on Fungal Genetics (ECFG13), April, 2016. Paris, France.

(Poster) “HFB8, the orphan-hydrophobin of Trichoderma guizhouense, is involved in mycoparasitism, surface growth and protects hyphae from fungicides”, The 14th European Conference on Fungal Genetics (ECFG14), February 2018. Haifa, Israel.

LANGUAGE SKILLS

Chinese                                         Native

English                                          Fluent

German                                         Basic

 LIST OF PUBLICATIONS

FIRST- AND CORRESPONDING-AUTHORED ARTICLES

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. Evolutionary compromises in fungal fitness: hydrophobins hinder the adverse dispersal of spores and challenge their survival. ISME J 14, 2610–2624 (2020). https://doi.org/10.1038/s41396-020-0709-0

Ding, M., Chen, W., Ma, X., Lv, B., 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. (in press, Journal of Applied Microbiology)

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

Cai, F., Pang, G., Li, R.-X., Li, R., Gu, X.-L., Shen, Q.-R., and Chen, W. 2017a. Bioorganic fertilizer maintains a more stable soil microbiome than chemical fertilizer for monocropping. Biology and Fertility of Soils. 53:861–872

Cai, F., Pang, G., Miao, Y., Li, R., Li, R., Shen, Q., and Chen, W. 2017b. The nutrient preference of plants influences their rhizosphere microbiome. Applied Soil Ecology. 110:146–150

Cai, F., Chen, W., Wei, Z., Pang, G., Li, R., Ran, W., and Shen, Q. 2015. Colonization of Trichoderma harzianum strain SQR-T037 on tomato roots and its relationship to plant growth, nutrient availability and soil microflora. Plant and Soil. 388:337–350

Li, R.-X., Cai, F., Pang, G., Shen, Q.-R., Li, R., and Chen, W. 2015. Solubilisation of phosphate and micronutrients by Trichoderma harzianum and its relationship with the promotion of tomato plant growth. PLoS ONE. 10:e0130081 (shared first authorship)

Cai, F., Yu, G., Wang, P., Wei, Z., Fu, L., Shen, Q., and Chen, W. 2013. Harzianolide, a novel plant growth regulator and systemic resistance elicitor from Trichoderma harzianum. Plant Physiology and Biochemistry. 73:106–113

CO-AUTHORED ARTICLES

Perez-Llano, Y., Rodriguez-Pupo, E.C., Druzhinina, I.S., Chenthamara, K., Cai, F., Gunde-Cimerman, N. et al. 2020. Stress reshapes the physiological response of halophile fungi to salinity. Cells 9.

Zhang, Y., Wang, X., Pang, G., Cai, F., Zhang, J., Shen, Z., Li, R., and Shen, Q., 2019. Two-step genomic sequence comparison strategy to design Trichoderma strain-specific primers for quantitative PCR. AMB Express 9: 179.

Zhang, J., Miao, Y., Rahimi, M.J., Zhu, H., Steindorff, A., Schiessler, S., Cai, F., Pang, G., Chenthamara, K., Xu, Y., Kubicek, C.P., Shen, Q., Druzhinina, I.S., 2019. Guttation capsules containing hydrogen peroxide: an evolutionarily conserved NADPH oxidase gains a role in wars between related fungi: The role of hydrogen peroxide in fungal wars. Environmental Microbiology.

Hatvani, L., Homa, M., Chenthamara, K., Cai, F., Kocsubé, S., Atanasova, L., Mlinaric-Missoni, E., Manikandan, P., Revathi, R., Dóczi, I., Iványi, B., Bogáts, G., Narendran, V., Büchner, R., Vágvölgyi, C., Druzhinina, I.S., Kredics, L. 2019. Agricultural systems as potential sources of emerging human mycoses caused by Trichoderma FEMS Microbiology Letters, in press

Jiang, S.-Q., Yu, Y.-N., Gao, R.-W., Wang, H., Zhang, J., Li, R., Long, X.-H., Shen, Q.-R., Chen, W., and Cai, F. 2019. High-throughput absolute quantification sequencing reveals the effect of different fertilizer applications on bacterial community in a tomato cultivated coastal saline soil. Science of the Total Environment. 687:601–609

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., and Druzhinina, I. S. 2019. Evolution and comparative genomics of the most common Trichoderma species. BMC Genomics. 20

Druzhinina, I. S., Chenthamara, K., Zhang, J., Atanasova, L., Yang, D., Miao, Y., Rahimi, M. J., Grujic, M., Cai, F., Pourmehdi, S., Salim, K. A., Pretzer, C., Kopchinskiy, A. G., Henrissat, B., Kuo, A., Hundley, H., Wang, M., Aerts, A., Salamov, A., Lipzen, A., LaButti, K., Barry, K., Grigoriev, I. V., Shen, Q., and Kubicek, C. P. 2018. Massive lateral transfer of genes encoding plant cell wall-degrading enzymes to the mycoparasitic fungus Trichoderma from its plant-associated hosts. PLOS Genetics. 14:e1007322

Pang, G., Cai, F., Li, R., Zhao, Z., Li, R., Gu, X., Shen, Q., and Chen, W. 2017. Trichoderma-enriched organic fertilizer can mitigate microbiome degeneration of monocropped soil to maintain better plant growth. Plant and Soil. 416:181–192

Przylucka, A., Akcapinar, G. B., Chenthamara, K., Cai, F., Grujic, M., Karpenko, J., Livoi, M., Shen, Q., Kubicek, C. P., and Druzhinina, I. S. 2017. HFB7 – A novel orphan hydrophobin of the Harzianum and Virens clades of Trichoderma, is involved in response to biotic and abiotic stresses. Fungal Genetics and Biology. 102:63–76

BOOK CHAPTERS

Chenthamara, K., Rahimi, M., Grujic, M., Druzhinina, I. S. and Cai, F.* Trichoderma reesei – Methods and Protocols: Ecological genomics and evolution of Trichoderma reesei, Mach-Aignar, A., and Martzy, R., eds. Methods in Molecular Biology, Springer Nature (in press)

Rahimi, M., Cai, F., Grujic, M., Chenthamara, K., andDruzhinina, I. S. Trichoderma reesei – Methods and Protocols: Molecular identification of Trichoderma reesei. Mach-Aigner, A. and Martzy, R., eds. Methods in Molecular Biology, Springer Nature (in press)

Cai, F., Kubicek, C. P., and Druzhinina, I. S. Biofuels and Biodiesel: Genetic transformation of Trichoderma spp. Chhandak B., ed. Methods in Molecular Biology, Springer Nature (in press)