Fungal metabolic plasticity and sexual development mediate induced resistance to arthropod fungivory

Abstract

ResearchCite this article: Döll K, Chatterjee S, Scheu S, Karlovsky P, Rohlfs M. Prey organisms do not tolerate predator attack passively but react with a multitude of inducible defensive strategies. Although inducible defence strategies are well known in plants attacked by herbivorous insects, induced resistance of fungi against fungivorous animals is largely unknown. Resistance to fungivory is thought to be mediated by chemical properties of fungal tissue, i.e. by production of toxic secondary metabolites. However, whether fungi change their secondary metabolite composition to increase resistance against arthropod fungivory is unknown. We demonstrate that grazing by a soil arthropod, Folsomia candida, on the filamentous fungus Aspergillus nidulans induces a phenotype that repels future fungivores and retards fungivore growth. Arthropod-exposed colonies produced significantly higher amounts of toxic secondary metabolites and invested more in sexual reproduction relative to unchallenged fungi. Compared with vegetative tissue and asexual conidiospores, sexual fruiting bodies turned out to be highly resistant against fungivory in facultative sexual A. nidulans. This indicates that fungivore grazing triggers co-regulated allocation of resources to sexual reproduction and chemical defence in A. nidulans. Plastic investment in facultative sex and chemical defence may have evolved as a fungal strategy to escape from predation.

Fungal Morphogenesis, from the Polarized Growth of Hyphae to Complex Reproduction and Infection Structures

“…Arthropod-exposed colonies produced significantly larger amounts of toxic secondary metabolites and invested more in sexual reproduction than did unchallenged fungi. Their results indicated that in A. nidulans, fungivore grazing triggered the coregulated allocation of resources to sexual reproduction and chemical defense (442). That same group established a mechanism of regulation through RsmA, a recently discovered YAP-like bZIP protein that impacts secondary metabolite production through the regulation of the C6 transcription factor aflR.…”

“…The production of toxic secondary metabolites is thought to mediate resistance to fungi-vory. However, whether fungi change their pattern of secondary metabolite production to increase resistance to fungivory remained an open question until recently, when Döll and coworkers (442) demonstrated that grazing by a soil arthropod, Folsomia candida, on A. nidulans induced a phenotype that repelled subsequent attacks and retarded fungivore growth. Arthropod-exposed colonies produced significantly larger amounts of toxic secondary metabolites and invested more in sexual reproduction than did unchallenged fungi.…”

Fungal Secondary Metabolism in the Light of Animal–Fungus Interactions: From Mechanism to Ecological Function

“…9.5). Döll et al [113] show changes in both morphology and chemistry of A. nidulans in response to grazing by the springtail F. candida (Fig. 9.1e).…”

“…Springtail-damaged colonies that were found to repel later-arriving fungivores contained significantly higher amounts of sterigmatocystin and produced a significantly greater number of sexual fruiting bodies. Springtails appeared to be able to adapt in the long term to more toxic colonies and consumed vegetative hyphae and conidia, however, they avoided feeding on cleistothecia including the surrounding layer of Hülle cells [113]. This combined and flexible investment in secondary metabolites and sexual reproduction probably is a strategy for fungal survival and persistence in predator-rich niches.…”

Fungal Secondary Metabolites in the “OMICS” Era

“…9). Examples include the specific expression of genes including the transcriptional regulator of sterigmatocystin biosynthesis aflR in A. nidulans upon attack by Drosophila melanogaster larvae [59]; the enhanced amounts of sterigmatocystin, emericellamides, and certain meroterpenoids in springtail-damaged A. nidulans colonies [60]; and the enhanced expression of the easB and ausA polyketide synthase genes in confrontation assays with fruit fly larvae [61,62].…”