Fungal defences against animal antagonists – lectins & more

Authors

  • FRANK KEMPKEN

    1. Abteilung für Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer Garten, Christian-Albrechts-Universität zu Kiel, Olshausenstr 40, 24098 Kiel, Germany
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  • PERSPECTIVE

Frank Kempken, Fax: +49 431 880 4248; E-mail: fkempken@bot.uni-kiel.de

Abstract

Unlike in the laboratory, in nature fungi are exposed to antagonists including competitors, pathogens, parasites and predators. In this issue of Molecular Ecology, an exciting paper by Bleuler-Martínez et al. (2011) has unearthed on one of the processes used by fungi to protect themselves against animal antagonists. The authors from Markus Künzler′s group at the ETH Zürich, Switzerland present direct evidence that filamentous fungi possess an inducible resistance mechanism against predators and parasites. This is based on cytoplasmic lectins, which specifically bind to glycans of these predators and parasites, and thus provide toxicity against them. These lectins are expressed at high levels in fruiting bodies and sclerotia of these fungi (Fig. 1). While there have been previous suggestions and efforts to implicate mycotoxins such as sterigmatocystin into fungal defence mechanisms and as an evolutionary force (see Kempken & Rohlfs 2010), the data presented by Markus Künzler′s group highlight the ecological relevance of lectins in defending fungi from parasites and fungivorous animals. As such this paper provides important ecological clues and suggests that secondary metabolites are not the sole player in fungal–animal competition. It rather appears that fungi have evolved several lines of defence against antagonistic organisms.

Figure 1.

 Fungi protect their fruiting bodies by the use of lectin (picture of Aleuria aurantia provided by Taylor F. Lockwood).

Fungal lectins have been long since known; however, their biological function remained elusive. They are found in many ascomycete and basidomycete fungi, which form fruiting bodies. Fruiting body lectins are small, water-soluble molecules in the cytoplasm. It should be mentioned that there are other types of lectins present in fungi, i.e. secreted ones which may have other biological functions. Some fruiting body lectins appear to have anti-tumour, anti-viral and immune-stimulating activities against mammalian cells, but this could not be considered to be their biological function. Fruiting body lectins have been thought to be involved in fungal morphogenesis or development based on their up-regulation during these processes. However, knock-outs did not have any effect on morphogenesis or development, and in fact exhibited no obvious phenotype at all. The cytoplasmic localization of fungal fruiting body lectins and the absence of fungal glycans to which these lectins may bind further are not in favour of an endogenous biological function in fungal metabolism or physiology (for lit. see Bleuler-Martínez et al. 2011).

Bleuler-Martínez et al. (2011) in this issue address the biological function by over-expressing in Escherichia coli different lectins from seven fruiting body forming ascomycete and basidiomycete fungi, and feeding these to three model predators or parasites, the nematode Caenorhabditis elegans, mosquito larvae of Aedes aegypti, and the amoeba Acanthamoeba castellanii. The rationale being, that using a wide variety of organisms from phyla with known fungivorous members would increase the ecological relevance of the data. Having the biotoxicity test procedure set up made previously (Künzler et al. 2010), six of the seven lectins were found to be toxic for at least two of the test organisms. Three lectins, TAP1 from Sordaria macrospora. CGL2 from Coprinopsis cinerea, and AAL from Aleuria aurantia were found to be toxic for all tested organisms. Although the amount of lectins fed was probably higher than in real mushroom tissue, the food choice experiments performed in the study confirm effects on the animals at much lower levels of lectin concentration. While lectin production is particularly high in fruiting bodies, it was even found to be induced in vegetative hyphae from C. cinerea upon confrontation with the fungivorous nematode Aphelenchus avenae. GFP-labelled cytoplasmic content of the fungus was found in the intestine of these nematodes, providing an explanation for the cytoplasmic localization of lectins so as to enhance delivery of toxic lectins to feeding animals. Clearly, the specificity of fruiting body lectins for binding to glycans from fungivorous and parasitic animals strongly argues for a role of these lectins as a defence mechanism against animal antagonists. However, the way lectin expression is induced in vegetative hyphae remains to be seen. It is possible that fungi can sense fungivory or at least fungivores feeding on hyphae.

This study is important in that it provides strong evidence for a new mechanism of defence against animal antagonists. So far interest has mainly focused on the extensive repertoire of toxic fungal secondary metabolites, well-known examples being penicillin or cephalosporin as effector molecules against bacterial antagonists (e.g. Schmitt et al. 2004). Other secondary metabolites are believed to provide protection against fungivory. In Aspergillus nidulans, the protein LaeA is a global regulator of secondary metabolite production (Bok & Keller 2004). Using a mutant deleted for LaeA, it was demonstrated that springtails prefer the LaeA mutant for feeding in food choice experiments. Springtails feeding on the LaeA mutant produced more offspring when compared with the wild type (Rohlfs et al. 2007). These results demonstrate that fungal secondary metabolites shape food choice behaviour and affect population dynamics of fungivores. That study also provides evidence for a selective force favouring secondary metabolites synthesis in fungi (Rohlfs et al. 2007). Finally a third group of proteins, fungal protease inhibitors with similar expression patterns and subcellular localization as fruiting body lectins appear to be involved in defence against animal antagonists (Avanzo et al. 2009).

So what is the take home message? (i) Filamentous fungi possess an inducible resistance against predators and parasites. This is based on fruiting body lectins which are specific for glycans of these predators and parasites. (ii) Secondary metabolites and fungal protease inhibitors appear to provide another important line of defence, and (iii) in the future, there is much more to learn from fungal–animal interactions and competitions.

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