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.
Highlights
There is an increasing consensus that microbial communities have an important role in mediating ecosystem processes
All soil enzyme activities presented the highest activity at site 3 and NAG and acid phosphatase (ACP) activities were found significantly lower at site 2 (Supplementary Table 2)
We further found that root functional traits were highly explained by the ECM community, which corroborates the important mediation role of ECM on plant status and performance, and the need of incorporating symbiotic traits into the analysis of root traits (Weemstra et al, 2016)
Summary
There is an increasing consensus that microbial communities have an important role in mediating ecosystem processes. The effect of plant hosts on their microbiomes has often been studied from a taxonomic point of view (Aponte et al, 2010; de Vries et al, 2012; Kurm et al, 2018), little is known about how soil microbial functional traits are affecting the functioning of plant species. It is debatable whether the features of microbes associated to individual plants (species composition and trait distribution) can be defined as plant traits, as they are not heritable features, according to the definition of Garnier et al (2016). Some authors have considered the use of traits in the root microbiome as an extension of the plant species phenotype for explaining functional changes in plant communities along environmental gradients and it has been included in a multidimensional root trait framework (NavarroFernández et al, 2016; Weemstra et al, 2016)
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