Evolutionary compromises in fungal fitness: hydrophobins can hinder the adverse dispersal of conidio
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 plasti
Source : The ISME Journal
Auth : Feng Cai, Renwei Gao, Zheng Zh
keywords : Aerial hyphae, Anemophilous spore dispersal, Biolo

Evolutionary compromises in fungal fitness: hydrophobins can hinder the adverse dispersal of conidiospores and challenge their survival

Running title: Role of HFBs in fungal fitness and speciation

Feng Cai1-3, Renwei Gao2, Zheng Zhao2, Mingyue Ding2, Siqi Jiang2, Civan Yagtu3, Hong Zhu2, Jian Zhang1,2, Thomas Ebner4, Michael Mayrhofer-Reinhartshuber4, Philipp Kainz4, Komal Chenthamara3, Günseli Bayram Akcapinar3,5, Qirong Shen1, *, Irina S. Druzhinina2,3, *

1Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Jiangsu Collaborative Innovation Center of Solid Organic Wastes, Educational Ministry Engineering Center of Resource-Saving Fertilizers, Nanjing Agricultural University, 210095, Nanjing, China

2Fungal Genomics Group, Nanjing Agricultural University, 210095, Nanjing, China

3Institute of Chemical, Environmental and Bioscience Engineering (ICEBE), TU Wien, A1060, Vienna, Austria

4KML Vision GmbH, A8020, Graz, Austria

5Acibadem Mehmet Ali Aydinlar University, Institute of Health Sciences, Department of Medical Biotechnology, Istanbul, Turkey

*Corresponding authors:

Irina S. Druzhinina, Nanjing Agricultural University, College of Resources and Environmental Sciences, Fungal Genomics Group, Weigang NO. 1, Nanjing, China, 210095, Tel +86 15 996344211, Fax +86 25 84396326 Email: irina.druzhinina@njau.edu.cn;

Qirong Shen, Nanjing Agricultural University, College of Resources and Environmental Sciences, Jiangsu Provincial Key Lab of Solid Organic Waste Utilization, Weigang NO. 1, Nanjing, China, 210095, Tel +86 84396291, Fax +86 25 84396291 Email: qirongshen@njau.edu.cn

Keywords

Aerial hyphae, Anemophilous spore dispersal, Biolog Phenotype MicroArrays, Conidiation, Ecological genetics, Hydrophobin, Positive selection, Pluviophilous spore dispersal, REPAINT, Small secreted cysteine-rich proteins, Speciation

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.


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