Environmental filtering primarily drives the composition of ectomycorrhizal fungal communities during ecological succession in the Mediterranean

In the western part of the Mediterranean basin, millenaries of anthropic pressure have converted landscapes into complex mosaics of habitats in which Quercus ilex forests fragments border on large patches of shrubby degraded vegetation locally called garrigues. While the fungal diversity established in forests have been extensively studied, the ability of plant community to host ectomycorrhizal (EM) diversity after disturbance remains poorly documented.

In these pioneer ecosystems facing severe drought, EM fungal diversity depends on the establishment of highly adapted species from the Cistaceae family, mainly from the Fumana and Helianthemum genera. In order to document the EM fungal diversity in Cistaceae-dominated garrigues, we used a [succession stage x plant species] crossed factor sampling scheme to compare communities established on roots of three species (Fumana ericifolia vs F. thymifolia vs Helianthemum oelandicum subsp. italicum) across three succession stages (dry Cistaceae grasslands vs Cistaceae garrigue vs oak secondary forest).

A dozen of EM root tips were sampled on each of 90 collected plant individuals and the ITS locus was successfully Sanger sequenced on 1036 root apices. Out of the 164 resulting OTUs phylogenetically analyzed, 84 were assigned to the EM guild, and 80% of them remain undescribed (67 taxa). The comparison of EM communities on these contrasted contexts reveals a high EM alpha diversity across succession stages and among host species. Highly stressful environments harbor remarkably rich EM communities, comparable with those from Cistaceae found in forests. We demonstrate that habitat acts as the main filter for EM beta diversity, followed by the identity of the plant host. The composition of EM communities in forests is dominated by corticioid Basidiomycota, while sequestrate Ascomycota account for the majority of taxa in early-successional vegetation stage.

This study sheds lights on the high potential of Mediterranean early-successional habitats for the conservation of a so far poorly known fungal diversity symbiotically associated to drought-tolerant plants submitted to highly selective environmental conditions. From a functional perspective, these extreme habitats and their highly specialized fungal diversity patterns provide ideal case study to explore the mechanisms underlying the maintenance of local hotspots of EM diversity.