Fungal microbiomes associated with Lycopodiaceae during ecological succession.

Abstract

Lycopodiaceae species form an early-diverging plant family, characterized by achlorophyllous and subterranean gametophytes that rely on mycorrhizal fungi for their nutrition. Lycopodiaceae often emerge after a disturbance, like in the Hochfeld reserve (Alsace, France) where seven lycopod species appeared on new ski trails following a forest cut. Here, to better understand their ecological dynamic, we conducted a germination experiment of lycopod spores following an anthropogenic disturbance and examined their associated fungi. Only 12% of the samples germinated, and all gametophytes were abundantly colonized by a specific clade of Densosporaceae (Endogonales, Mucoromycotina), which were also present in the roots of lycopod sporophytes, but absent from the ungerminated spores and the roots of surrounding herbaceous plants, suggesting high mycorrhizal specificity in Lycopodiaceae. In addition, ungerminated spores were profusely parasitized by chytrid fungi, also present in the surrounding lycopod gametophytes and sporophytes, which might explain the low spore germination rate. Altogether, the requirement of specific mycorrhizal Mucoromycotina fungi and the high prevalence of parasites may explain why Lycopodiaceae are often rare pioneer species in temperate regions, limited to the first stages of ecological succession. This illustrates the primordial roles that belowground microbes play in aboveground plant dynamics.