Spatial structure and growth dynamics of fairy rings formed by Marasmius oreades

Abstract

Despite the long-term fascination of fairy ring-forming fungi, many aspects of their biology remain unresolved. It is not known why the mycelium grows as an annular structure, rather than a solid disc, or why it grows radially outwards. Different theories have been suggested, but none have been tested experimentally with molecular resolution. Here, we undertook a metagenomic approach to study the growth dynamics of the fairy ring-forming fungus Marasmius oreades. We confirmed that M. oreades grows as an open ring by detecting its DNA in metagenomes of soil collected along transects from two fairy rings. We showed that the mycelia forming rings are dikaryotic by identifying two mating-type alleles and showing genome-wide heterozygosity. We tested five hypotheses for the mechanism of radial outgrowth using transplantation experiments. The results were most consistent with a transient-escape hypothesis, and suggest that the mycelium avoids inhibitory factors present at the back edge of the mycelial growth front. Our study demonstrates the power of metagenomics for studying fungi, showing that detailed genomic information can be recovered directly from soil. This approach enables the investigation of cryptic aspects of fungal biology, such as the growth of fairy ring-forming fungi, in natural settings that would otherwise remain hidden.