Secondary metabolites of Hülle cells mediate protection of fungal reproductive and overwintering structures against fungivorous animals

Abstract

Fungal Hülle cells with nuclear storage and developmental backup functions are reminiscent of multipotent stem cells. In the soil, Hülle cells nurse the overwintering fruiting bodies of Aspergillus nidulans. The genome of A. nidulans harbors genes for the biosynthesis of xanthones. We show that enzymes and metabolites of this biosynthetic pathway accumulate in Hülle cells under the control of the regulatory velvet complex, which coordinates development and secondary metabolism. Deletion strains blocked in the conversion of anthraquinones to xanthones accumulate emodins and are delayed in maturation and growth of fruiting bodies. Emodin represses fruiting body and resting structure formation in other fungi. Xanthones are not required for sexual development but exert antifeedant effects on fungivorous animals such as springtails and woodlice. Our findings reveal a novel role of Hülle cells in establishing secure niches for A. nidulans by accumulating metabolites with antifeedant activity that protect reproductive structures from animal predators.

Orchestrated Biosynthesis of the Secondary Metabolite Cocktails Enables the Producing Fungus to Combat Diverse Bacteria

“…For example, the biosynthesis of cyclodepsipeptide destruxins is required for the virulence of Metarhizium by the evasion of insect immune responses ( 31 ). The bis-naphthopyrone aurofusarin produced by Fusarium and the xanthones produced by A. nidulans can protect the producing fungi from a wide range of invertebrate predators ( 32 , 33 ). The bibenzoquinone oosporein produced by B. bassiana could assist with the fungal infection of insects and limit the in insecta bacterial growth after the fungal killing of the insects ( 34 , 35 ).…”

Biosynthesis of Antibacterial Iron-Chelating Tropolones in Aspergillus nidulans as Response to Glycopeptide-Producing Streptomycetes

“…well as their predators (Linares et al, 2006;Granato et al, 2019;Gerke et al, 2020;Liu et al, 2021). Fungi and bacteria are in a continuous rivalry in consumption of substrates in soil (Boer et al, 2005).…”

Fungal Melanin Biosynthesis Pathway as Source for Fungal Toxins

“…Secondary metabolites are not only used to treat human and animal infections (e.g., penicillins, griseofulvin) or diseases (e.g., lovastatin) but also as fungicides for plant protection (e.g., strobilurins) ( 4 , 5 ). Most filamentous fungi produce a blend of different metabolites, for most of which their natural function is still unknown and not so easy to decipher ( 6 , 7 ). Meanwhile, hundreds of fungal genomes have been sequenced, and most contain a large number of genes encoding enzymes for secondary metabolite biosynthesis ( 8 , 9 ).…”

“…However, since the discovery of the biosynthesis of aflatoxin and the corresponding gene cluster, many variations have been described ( 18 ). For instance, in the case of meroterpenoids or xanthones, two separate gene clusters are required for their biosynthesis ( 6 , 19 ). Another example is the nematode-trapping fungus Duddingtonia flagrans , where the expression of some cluster genes is spatially regulated, resulting in different metabolites at different places in the mycelium ( 20 ).…”