Comparative Analysis of Secretomes from Ectomycorrhizal Fungi with an Emphasis on Small-Secreted Proteins.

Clement Pellegrin,Claire Veneault-Fourrey,Emmanuelle Morin,Francis M Martin

doi:10.3389/fmicb.2015.01278

Clement Pellegrin, Claire Veneault-Fourrey + Show 2 more

Open Access

https://doi.org/10.3389/fmicb.2015.01278

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Abstract

Fungi are major players in the carbon cycle in forest ecosystems due to the wide range of interactions they have with plants either through soil degradation processes by litter decayers or biotrophic interactions with pathogenic and ectomycorrhizal symbionts. Secretion of fungal proteins mediates these interactions by allowing the fungus to interact with its environment and/or host. Ectomycorrhizal (ECM) symbiosis independently appeared several times throughout evolution and involves approximately 80% of trees. Despite extensive physiological studies on ECM symbionts, little is known about the composition and specificities of their secretomes. In this study, we used a bioinformatics pipeline to predict and analyze the secretomes of 49 fungal species, including 11 ECM fungi, wood and soil decayers and pathogenic fungi to tackle the following questions: (1) Are there differences between the secretomes of saprophytic and ECM fungi? (2) Are small-secreted proteins (SSPs) more abundant in biotrophic fungi than in saprophytic fungi? and (3) Are there SSPs shared between ECM, saprotrophic and pathogenic fungi? We showed that the number of predicted secreted proteins is similar in the surveyed species, independently of their lifestyle. The secretome from ECM fungi is characterized by a restricted number of secreted CAZymes, but their repertoires of secreted proteases and lipases are similar to those of saprotrophic fungi. Focusing on SSPs, we showed that the secretome of ECM fungi is enriched in SSPs compared with other species. Most of the SSPs are coded by orphan genes with no known PFAM domain or similarities to known sequences in databases. Finally, based on the clustering analysis, we identified shared- and lifestyle-specific SSPs between saprotrophic and ECM fungi. The presence of SSPs is not limited to fungi interacting with living plants as the genome of saprotrophic fungi also code for numerous SSPs. ECM fungi shared lifestyle-specific SSPs likely involved in symbiosis that are good candidates for further functional analyses.

Highlights

In forest ecosystems, tree roots are continuously in contact with beneficial, commensal and pathogenic soil microbes
To determine whether secretomes and small-secreted proteins (SSPs) are related to biotrophic or saprotrophic lifestyles, we developed a pipeline to identify and compare the secretome from 49 fungal fungi including 41 Basidiomycota, six Ascomycota, one Zygomycota, and one Chytridiomycota (Figure 1, Table 1)
The results should be taken with care as they may be impacted by both qualities of sequencing (Supplementary Data sheet 3) and annotation tools used

Summary

Introduction

In forest ecosystems, tree roots are continuously in contact with beneficial, commensal and pathogenic soil microbes. The root microbiome is driving forest health, productivity and sustainability (Wagg et al, 2014) Among those microorganisms, fungi stand as key players that demonstrate a wide range of interactions with plants. The tree supplies the ECM fungus with up to 30% of its photosynthesis-derived carbohydrates in return for up to 70% of its N and P needs, which are received from the ECM hyphal networks that extend deep within the soil (Nehls, 2008; Martin and Nehls, 2009) This mutualistic interaction relies on a constant nutrient exchanges between partners and contributes to better tree growth and health by improving mineral nutrition, strengthening plant defenses and directly contributing to the exclusion of competitive microbes (Wallander et al, 2001; Franklin et al, 2014)

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