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      Fungal diversity regulates plant-soil feedbacks in temperate grassland

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          Abstract

          Plant growth dynamics are shaped by the diversity of associating pathogenic, saprotrophic, and mutualistic soil fungi.

          Abstract

          Feedbacks between plants and soil microbial communities play an important role in vegetation dynamics, but the underlying mechanisms remain unresolved. Here, we show that the diversity of putative pathogenic, mycorrhizal, and saprotrophic fungi is a primary regulator of plant-soil feedbacks across a broad range of temperate grassland plant species. We show that plant species with resource-acquisitive traits, such as high shoot nitrogen concentrations and thin roots, attract diverse communities of putative fungal pathogens and specialist saprotrophs, and a lower diversity of mycorrhizal fungi, resulting in strong plant growth suppression on soil occupied by the same species. Moreover, soil properties modulate feedbacks with fertile soils, promoting antagonistic relationships between soil fungi and plants. This study advances our capacity to predict plant-soil feedbacks and vegetation dynamics by revealing fundamental links between soil properties, plant resource acquisition strategies, and the diversity of fungal guilds in soil.

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          Most cited references31

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          Soil biodiversity and soil community composition determine ecosystem multifunctionality.

          Biodiversity loss has become a global concern as evidence accumulates that it will negatively affect ecosystem services on which society depends. So far, most studies have focused on the ecological consequences of above-ground biodiversity loss; yet a large part of Earth's biodiversity is literally hidden below ground. Whether reductions of biodiversity in soil communities below ground have consequences for the overall performance of an ecosystem remains unresolved. It is important to investigate this in view of recent observations that soil biodiversity is declining and that soil communities are changing upon land use intensification. We established soil communities differing in composition and diversity and tested their impact on eight ecosystem functions in model grassland communities. We show that soil biodiversity loss and simplification of soil community composition impair multiple ecosystem functions, including plant diversity, decomposition, nutrient retention, and nutrient cycling. The average response of all measured ecosystem functions (ecosystem multifunctionality) exhibited a strong positive linear relationship to indicators of soil biodiversity, suggesting that soil community composition is a key factor in regulating ecosystem functioning. Our results indicate that changes in soil communities and the loss of soil biodiversity threaten ecosystem multifunctionality and sustainability.
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            Microbial diversity drives multifunctionality in terrestrial ecosystems

            Despite the importance of microbial communities for ecosystem services and human welfare, the relationship between microbial diversity and multiple ecosystem functions and services (that is, multifunctionality) at the global scale has yet to be evaluated. Here we use two independent, large-scale databases with contrasting geographic coverage (from 78 global drylands and from 179 locations across Scotland, respectively), and report that soil microbial diversity positively relates to multifunctionality in terrestrial ecosystems. The direct positive effects of microbial diversity were maintained even when accounting simultaneously for multiple multifunctionality drivers (climate, soil abiotic factors and spatial predictors). Our findings provide empirical evidence that any loss in microbial diversity will likely reduce multifunctionality, negatively impacting the provision of services such as climate regulation, soil fertility and food and fibre production by terrestrial ecosystems.
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              Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients

              Terrestrial ecosystems are receiving elevated inputs of nitrogen (N) from anthropogenic sources and understanding how these increases in N availability affect soil microbial communities is critical for predicting the associated effects on belowground ecosystems. We used a suite of approaches to analyze the structure and functional characteristics of soil microbial communities from replicated plots in two long-term N fertilization experiments located in contrasting systems. Pyrosequencing-based analyses of 16S rRNA genes revealed no significant effects of N fertilization on bacterial diversity, but significant effects on community composition at both sites; copiotrophic taxa (including members of the Proteobacteria and Bacteroidetes phyla) typically increased in relative abundance in the high N plots, with oligotrophic taxa (mainly Acidobacteria) exhibiting the opposite pattern. Consistent with the phylogenetic shifts under N fertilization, shotgun metagenomic sequencing revealed increases in the relative abundances of genes associated with DNA/RNA replication, electron transport and protein metabolism, increases that could be resolved even with the shallow shotgun metagenomic sequencing conducted here (average of 75 000 reads per sample). We also observed shifts in the catabolic capabilities of the communities across the N gradients that were significantly correlated with the phylogenetic and metagenomic responses, indicating possible linkages between the structure and functioning of soil microbial communities. Overall, our results suggest that N fertilization may, directly or indirectly, induce a shift in the predominant microbial life-history strategies, favoring a more active, copiotrophic microbial community, a pattern that parallels the often observed replacement of K-selected with r-selected plant species with elevated N.
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                Author and article information

                Journal
                Sci Adv
                Sci Adv
                SciAdv
                advances
                Science Advances
                American Association for the Advancement of Science
                2375-2548
                November 2018
                28 November 2018
                : 4
                : 11
                : eaau4578
                Affiliations
                [1 ]School of Earth and Environmental Sciences, Michael Smith Building, The University of Manchester, Oxford Road, Manchester M13 9PT, UK.
                [2 ]Cooperative Institute for Research in Environmental Sciences, University of Colorado, Boulder, CO 80309, USA.
                [3 ]Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO 80309, USA.
                [4 ]Freie Universität Berlin, Institut für Biologie, Plant Ecology, D-14195 Berlin, Germany.
                [5 ]Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), D-14195 Berlin, Germany.
                [6 ]Institute of Ecology and Earth Sciences, The University of Tartu, Lai 40, 51005 Tartu, Estonia.
                [7 ]The Global Academy of Agriculture and Food Security, The Royal (Dick) School of Veterinary Studies, The University of Edinburgh, Midlothian EH25 9RG, UK.
                [8 ]Department of Terrestrial Ecology, Netherlands Institute of Ecology, P.O. Box 50, 6700 AB Wageningen, Netherlands.
                [9 ]Centre for Ecology & Hydrology, Lancaster Environment Centre, Library Avenue, Bailrigg, Lancaster LA1 4AP, UK.
                [10 ]Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK.
                Author notes
                [* ]Corresponding author. Email: marina.semchenko@ 123456manchester.ac.uk
                Author information
                http://orcid.org/0000-0001-6196-3562
                http://orcid.org/0000-0003-3309-2709
                http://orcid.org/0000-0002-0967-8219
                http://orcid.org/0000-0002-0161-6195
                http://orcid.org/0000-0001-6405-8111
                http://orcid.org/0000-0002-9864-6007
                http://orcid.org/0000-0002-7951-4818
                http://orcid.org/0000-0002-5757-7420
                http://orcid.org/0000-0003-3426-3178
                http://orcid.org/0000-0002-6432-4261
                Article
                aau4578
                10.1126/sciadv.aau4578
                6261650
                30498781
                970d2ef5-bf4b-4e76-bc25-be22d550aca4
                Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution License 4.0 (CC BY).

                This is an open-access article distributed under the terms of the Creative Commons Attribution license, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                : 12 June 2018
                : 25 October 2018
                Funding
                Funded by: doi http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: DEB 1542653
                Funded by: doi http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: Grant BB/I009000/2
                Funded by: doi http://dx.doi.org/10.13039/501100000268, Biotechnology and Biological Sciences Research Council;
                Award ID: BB/L026406/1
                Funded by: doi http://dx.doi.org/10.13039/501100000770, University Of Manchester;
                Funded by: doi http://dx.doi.org/10.13039/501100008530, European Regional Development Fund;
                Funded by: Government of Andalusia;
                Award ID: P09-RNM-04821
                Funded by: Kristjan Jaak Foundation;
                Categories
                Research Article
                Research Articles
                SciAdv r-articles
                Ecology
                Ecology
                Custom metadata
                Nielsen Marquez

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