Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils

Abstract

There is an increasing consensus that microbial communities have an important role in mediating ecosystem processes. Trait-based ecology predicts that the impact of the microbial communities on ecosystem functions will be mediated by the expression of their traits at community level. The link between the response of microbial community traits to environmental conditions and its effect on plant functioning is a gap in most current microbial ecology studies. In this study, we analyzed functional traits of ectomycorrhizal fungal species in order to understand the importance of their community assembly for the soil–plant relationships in holm oak trees (Quercus ilex subsp. ballota) growing in a gradient of exposure to anthropogenic trace element (TE) contamination after a metalliferous tailings spill. Particularly, we addressed how the ectomycorrhizal composition and morphological traits at community level mediate plant response to TE contamination and its capacity for phytoremediation. Ectomycorrhizal fungal taxonomy and functional diversity explained a high proportion of variance of tree functional traits, both in roots and leaves. Trees where ectomycorrhizal fungal communities were dominated by the abundant taxa Hebeloma cavipes and Thelephora terrestris showed a conservative root economics spectrum, while trees colonized by rare taxa presented a resource acquisition strategy. Conservative roots presented ectomycorrhizal functional traits characterized by high rhizomorphs formation and low melanization which may be driven by resource limitation. Soil-to-root transfer of TEs was explained substantially by the ectomycorrhizal fungal species composition, with the highest transfer found in trees whose roots were colonized by Hebeloma cavipes. Leaf phosphorus was related to ectomycorrhizal species composition, specifically higher leaf phosphorus was related to the root colonization by Thelephora terrestris. These findings support that ectomycorrhizal fungal community composition and their functional traits mediate plant performance in metal-contaminated soils, and have a high influence on plant capacity for phytoremediation of contaminants. The study also corroborates the overall effects of ectomycorrhizal fungi on ecosystem functioning through their mediation over the plant economics spectrum.

Evidence of pyrite dissolution by Telephora terrestris Ehrh in the Libiola mine (Sestri Levante, Liguria, Italy)

“…Mycorrhizal fungi are recognized for their importance for plant foraging of soil resources [20]: however, how mycorrhizal traits mediate soil-plant relationships is still an open question [24]. In the Libiola mine, ECM fungi enhance maritime pine nutrition, stress tolerance and soil structure and, consequently, promote the recovery of the vital functions in the degraded soil of the waste-rock dump.…”

“…Moreover, the success of P. pinaster as invader of eroded disturbed soils such as those occurring at the Libiola mine, may be attributed in part to its compatibility with many different ECM fungi [19], such as Telephora terrestris and Scleroderma polyrhizum . In fact, mycorrhyza-root association improves plant health helping the plant to resist stress caused by heavy metals as well as drought, salinity, and pathogens [20]. Moreover, other investigations [16, 21] demonstrated that these ECM macrofungi are able to accumulate high levels of metals, in particular Cu > 1000 mg/kg in Telephora terrestris and Ag>50000 μg/kg in Scleroderma polyrhizum .…”

Trace elements and C and N isotope composition in two mushroom species from a mine-spill contaminated site

“…A previous study in Sweden found fungi were able to take up and accumulate trace elements such as Cd, Cu and Zn in both sporocarps and mycelium (BCF from 1.9 to 8.8) in respect of bulk soil concentrations 56 . In this study, we found that the fungal uptake of trace elements is dependent on both the chemical element and the fungal species 5 . Low selectivity of fungal transporters for essential elements, such as Ca and Zn, favoured the transport of toxic ions with similar chemical properties, such as Cd 22 .…”

“…This fungal species has a wide ectomycorrhizal host potential, a low specificity and it is characteristic of young stands of trees 77 . This species has been identified as component of the fungal ectomycorrhizal communities associated with Quercus ilex in the study Scientific RepoRtS | (2020) 10:6434 | https://doi.org/10.1038/s41598-020-63194-2 www.nature.com/scientificreports www.nature.com/scientificreports/ area 5,78 . Volvopluteus gloiocephalus is distributed in Europe and North America and has bigger fruiting bodies than Laccaria laccata with white or grey-brown colours 79 .…”

Comparación entre las abundancias de esporomas y ectomicorrizas del género Laccaria en Ixtlán de Juárez, Oaxaca

“…Las comunidades microbianas del suelo presentan un papel importante en la mediación de los procesos del ecosistema, estas interacciones ecológicas y fisiológicas entre los organismos, están determinadas por factores bióticos y abióticos. Las plantas han desarrollado diferentes adaptaciones para contrarrestar sus limitaciones nutricionales, estrés hídrico, resistencia a patógenos o contaminantes (Gil-Martínez et al, 2018;Martin et al, 2008;Smith y Read, 2008). Una de las estrategias, es el establecer asociaciones mutualistas con microorganismos, como bacterias y hongos en las raíces; lo que se logra, entre otros mecanismos, a través de los exudados de las raíces que regulan las comunidades microbianas facilitando la simbiosis mutualista (Bais et al, 2004;Sanon et al, 2009).…”