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

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 betwee...

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Main Authors: Marta Gil-Martínez, Álvaro López-García, María T. Domínguez, Carmen M. Navarro-Fernández, Rasmus Kjøller, Mark Tibbett, Teodoro Marañón
Format: Article
Language:English
Published: Frontiers Media S.A. 2018-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2018.01682/full
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author Marta Gil-Martínez
Álvaro López-García
María T. Domínguez
Carmen M. Navarro-Fernández
Rasmus Kjøller
Mark Tibbett
Teodoro Marañón
author_facet Marta Gil-Martínez
Álvaro López-García
María T. Domínguez
Carmen M. Navarro-Fernández
Rasmus Kjøller
Mark Tibbett
Teodoro Marañón
author_sort Marta Gil-Martínez
collection DOAJ
description 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.
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spelling doaj.art-1a3cfeff8b9f446f8442f87cdf9f035f2022-12-22T03:08:29ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2018-11-01910.3389/fpls.2018.01682408149Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated SoilsMarta Gil-Martínez0Álvaro López-García1María T. Domínguez2Carmen M. Navarro-Fernández3Rasmus Kjøller4Mark Tibbett5Teodoro Marañón6Department for Protection of the Soil, Plant and Water System, Institute of Natural Resources and Agrobiology of Seville, Spanish National Research Council, Seville, SpainDepartment of Biology, University of Copenhagen, Copenhagen, DenmarkÁrea de Edafología y Química Agricola, Departamento de Cristalografía, Mineralogía y Química Agrícola, Universidad de Sevilla, Seville, SpainDepartment for Protection of the Soil, Plant and Water System, Institute of Natural Resources and Agrobiology of Seville, Spanish National Research Council, Seville, SpainDepartment of Biology, University of Copenhagen, Copenhagen, DenmarkCentre for Agri-Environmental Research and Soil Research Centre, School of Agriculture, Policy and Development, University of Reading, Reading, United KingdomDepartment for Protection of the Soil, Plant and Water System, Institute of Natural Resources and Agrobiology of Seville, Spanish National Research Council, Seville, SpainThere 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.https://www.frontiersin.org/article/10.3389/fpls.2018.01682/fullecosystem processesheavy metalmicrobiomephytoremediationQuercus ilex subsp. ballota (holm oak)root economics spectrum
spellingShingle Marta Gil-Martínez
Álvaro López-García
María T. Domínguez
Carmen M. Navarro-Fernández
Rasmus Kjøller
Mark Tibbett
Teodoro Marañón
Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils
Frontiers in Plant Science
ecosystem processes
heavy metal
microbiome
phytoremediation
Quercus ilex subsp. ballota (holm oak)
root economics spectrum
title Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils
title_full Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils
title_fullStr Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils
title_full_unstemmed Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils
title_short Ectomycorrhizal Fungal Communities and Their Functional Traits Mediate Plant–Soil Interactions in Trace Element Contaminated Soils
title_sort ectomycorrhizal fungal communities and their functional traits mediate plant soil interactions in trace element contaminated soils
topic ecosystem processes
heavy metal
microbiome
phytoremediation
Quercus ilex subsp. ballota (holm oak)
root economics spectrum
url https://www.frontiersin.org/article/10.3389/fpls.2018.01682/full
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