Compositions of fungal secretomes indicate a greater impact of phylogenetic history than lifestyle adaptation

Abstract

BackgroundSince the first fungal genome sequences became available, investigators have been employing comparative genomics to understand how fungi have evolved to occupy diverse ecological niches. The secretome, i.e. the entirety of all proteins secreted by an organism, is of particular importance, as by these proteins fungi acquire nutrients and communicate with their surroundings.ResultsIt is generally assumed that fungi with similar nutritional lifestyles have similar secretome compositions. In this study, we test this hypothesis by annotating and comparing the soluble secretomes, defined as the sets of proteins containing classical signal peptides but lacking transmembrane domains of fungi representing a broad diversity of nutritional lifestyles. Secretome size correlates with phylogeny and to a lesser extent with lifestyle. Plant pathogens and saprophytes have larger secretomes than animal pathogens. Small secreted cysteine-rich proteins (SSCPs), which may comprise many effectors important for the interaction of plant pathogens with their hosts, are defined here to have a mature length of ≤ 300 aa residues, at least four cysteines, and a total cysteine content of ≥5%. SSCPs are found enriched in the secretomes of the Pezizomycotina and Basidiomycota in comparison to Saccharomycotina. Relative SSCP content is noticeably higher in plant pathogens than in animal pathogens, while saprophytes were in between and closer to plant pathogens. Expansions and contractions of gene families and in the number of occurrences of functional domains are largely lineage specific, e.g. contraction of glycoside hydrolases in Saccharomycotina, and are only weakly correlated with lifestyle. However, within a given lifestyle a few general trends exist, such as the expansion of secreted family M14 metallopeptidases and chitin-binding proteins in plant pathogenic Pezizomycotina.ConclusionsWhile the secretomes of fungi with similar lifestyles share certain characteristics, the expansion and contraction of gene families is largely lineage specific, and not shared among all fungi of a given lifestyle.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-722) contains supplementary material, which is available to authorized users.

Comparative and transcriptional analysis of the predicted secretome in the lignocellulose‐degrading basidiomycete fungus Pleurotus ostreatus

“…The cluster of BR and ECM supports previous studies showing similarities in their organic matter degradation mechanisms (Rineau et al ., ) and a parallel contraction of the lignin‐degrading peroxidase gene family (Floudas et al ., ; Kohler et al ., ). The groups formed in this analysis reflected the fungal lifestyle rather than their evolutionary relationships, supporting the hypothesis that the fungal secretome could be used to predict the lifestyle because it is targeted to the ecological niche of the organism (Martinez et al ., ; Lowe and Howlett, ; Alfaro et al ., ; Krijger et al ., ). Two species of the genus Amanita [ A. thiersii (Hess et al ., ) and A. muscaria (Kohler et al ., )] with different lifestyles were included in this analysis; they appeared to be grouped according to their lifestyle rather than their phylogenetic classification.…”

“…Indeed, a blind grouping of organisms using their secretomes as distinctive characteristics produces a dendrogram in which the fungi are grouped by their lifestyle rather than by their phylogeny. Taken together, these data emphasize the dynamic, environmentally dependent, and ecologically influenced characteristics of fungal secretomes (Martinez et al ., ; Lowe and Howlett, ; Alfaro et al ., ; Krijger et al ., ).…”

Comparative systems analysis of the secretome of the opportunistic pathogen Aspergillus fumigatus and other Aspergillus species

“…The SSPs were then 16 evaluated for effector-like properties based on their EffectorP 81 (http://effectorp.csiro.au/) predictions or cysteine-richness. For identifying effector-like SSPs, cysteine-rich sequences are those which contain at least 4 cysteine residues and have greater than 5% of their total amino acid residues as cysteines 20,132 . The predicted SSPs in the secretomes of Aspergillus species were also scanned for known fungal or oomycetes effector motifs 80 Table S4).…”

Seeking the Roles for Fungal Small-Secreted Proteins in Affecting Saprophytic Lifestyles

“…The success of fungi to adapt and proliferate in diverse ecological niches is dependent on their ability to respond to changes in the environment. The rich, yet versatile, fungal secretome is an important component that facilitates the fast adjustment to changes occurring in the vicinity of the growing and developing fungus (Krijger et al, 2014;McCotter et al, 2016). The size of the secretome is 4-15% of the total gene number (Girard et al, 2013;Pellegrin et al, 2015).…”