Fungal secondary metabolite dynamics in fungus-grazer interactions: novel insights and unanswered questions

Abstract

In response to fungivore grazing fungi are assumed to have evolved secondary metabolite-based defense mechanisms that harm and repel grazers, and hence provide a benefit to the metabolite producer. However, since research into the ecological meaning of highly diverse fungal secondary metabolites is still in its infancy, many central questions still remain. Which components of the enormous metabolite diversity of fungi act as direct chemical defense mechanisms against grazers? Is the proposed chemical defense of fungi induced by grazer attack? Which role do volatile compounds play in communicating noxiousness to grazers? What is the relative impact of grazers and that of interactions with competing microbes on the evolution of fungal secondary metabolism? Here, I briefly summarize and discuss the results of the very few studies that have tried to tackle some of these questions by (i) using secondary metabolite mutant fungi in controlled experiments with grazers, and by (ii) investigating fungal secondary metabolism as a flexible means to adapt to grazer-rich niches.

Keywords: Aspergillus; chemical defense regulation; fungivory; inducible resistance; secondary metabolites.

FIGURE 1

Images depicting the localized formation of guttation droplets on the sexual fruiting bodies (cleistothecia) of A. nidulans, which are possibly involved in mediating protection from grazing by Collembola (see Döll et al., 2013). (A) To the left of the initial stage (primodium) of a cleistothecium (asterisk) a strikingly large droplet (arrow) is formed in addition to some smaller ones. The whitish appearance of the primordium is due to layers of so-called Hülle cells which are assumed to nurse and protect the developing ascospores within the cleistothecium. It is not obvious whether the guttation droplets are produced by the Hülle cells or aerial hyphae surrounding the fruiting bodies. (B) A cluster of larger cleistothecia (asterisk), surrounded by a dark mat of conidia-producing tissue. The cluster is covered by voluminous droplets of light-brown color (arrow). Numerous smaller and apparently colorless droplets attached to single aerial hyphae are also visible.

FIGURE 2

Scheme summarizing the results of some recent studies demonstrating a grazer-induced defense response in the model fungus Aspergillus nidulans [see text and publications by Döll et al. (2013) and Caballero Ortiz et al. (2013) for details]. This scheme may serve as a modifiable blueprint for future studies providing evidence for or against an inducible chemical defense in fungi, add more specific information from other fungal systems, or contribute to general, system-independent properties of fungal chemical responses to grazers, e.g., hormone and pheromone signaling. Although not indicated in detail, it should also be specified how both putative defense compounds affect fungivore behavior and physiology, to be better able to determine the ecological consequences of fungal secondary metabolites (SM) biosynthesis and hence the selective forces that may have, at least in part, shaped fungal SM diversity.