Phosphorus (P) acquisition is key for plant growth. Arbuscular mycorrhizal fungi (AMF) help plants acquire P from soil. Understanding which factors drive AMF-supported nutrient uptake is essential to develop more sustainable agroecosystems. Here we collected soils from 150 cereal fields and 60 non-cropped grassland sites across a 3,000 km trans-European gradient. In a greenhouse experiment, we tested the ability of AMF in these soils to forage for the radioisotope 33P from a hyphal compartment. AMF communities in grassland soils were much more efficient in acquiring 33P and transferred 64% more 33P to plants compared with AMF in cropland soils. Fungicide application best explained hyphal 33P transfer in cropland soils. The use of fungicides and subsequent decline in AMF richness in croplands reduced 33P uptake by 43%. Our results suggest that land-use intensity and fungicide use are major deterrents to the functioning and natural nutrient uptake capacity of AMF in agroecosystems.

Agroscope Division of Agroecology and Environment Plant Soil Interactions Group Zürich Switzerland

Berlin Brandenburg Institute of Advanced Biodiversity Research Berlin Germany

Departamento de Biología y Geología Física y Química Inorgánica Universidad Rey Juan Carlos Móstoles Madrid Spain

Departamento de Ecología Universidad de Alicante Alicante Spain

Departamento de Farmacología Farmacognosia y Botánica Facultad de Farmacia Universidad Complutense de Madrid Madrid Spain

Department of Agroecology University Bourgogne Franche Comte INRAE AgroSup Dijon Dijon France

Department of Forest Mycology and Plant Pathology Swedish University of Agricultural Sciences Uppsala Sweden

Department of Microbiological Sciences North Dakota State University Fargo ND USA

Department of Plant and Microbial Biology University of Zürich Zürich Switzerland

ETH Zürich Institute of Agricultural Sciences Group of Plant Nutrition Lindau Switzerland

Freie Universität Berlin Institute of Biology Berlin Germany

Institute of Microbiology Czech Academy of Sciences Prague Czech Republic

Instituto de Ciencias Agrarias Consejo Superior de Investigaciones Científicas Madrid Spain

Instituto Multidisciplinar para el Estudio del Medio 'Ramón Margalef' Universidad de Alicante Alicante Spain

Soil Science and Environment Group Changins University of Applied Sciences and Arts Western Switzerland Nyon Switzerland

Zobrazit více v PubMed

Foley JA, et al. Solutions for a cultivated planet. Nature. 2011;478:337–342. PubMed

Tilman D, Balzer C, Hill J, Befort BL. Global food demand and the sustainable intensification of agriculture. 2011;108:20260–20264. PubMed PMC

Bender SF, Wagg C, van der Heijden MGA. An Underground Revolution: Biodiversity and Soil Ecological Engineering for Agricultural Sustainability. Trends Ecol Evol. 2016;31:440–452. PubMed

Tamburini G, et al. Agricultural diversification promotes multiple ecosystem services without compromising yield. Sci Adv. 2020;6 PubMed PMC

Smith S, Read D. Mycorrhizal Symbiosis Mycorrhizal Symbiosis. Elsevier; 2008. DOI

Soudzilovskaia NA, et al. Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob Ecol Biogeogr. 2015;24:371–382.

Van Der Heijden MGA, Bardgett RD, Van Straalen NM. The unseen majority: Soil microbes as drivers of plant diversity and productivity in terrestrial ecosystems. Ecol Lett. 2008;11:296–310. PubMed

Bennett EM, Carpenter SR, Caraco NF. Human impact on erodable phosphorus and eutrophication: A global perspective. Bioscience. 2001;51:227–234.

Smith VH, Schindler DW. Eutrophication science: where do we go from here? Trends Ecol Evol. 2009;24:201–207. PubMed

Rillig MC, Mummey DL. Mycorrhizas and soil structure. New Phytol. 2006;171:41–53. PubMed

Bender SF, van der Heijden MGA. Soil biota enhance agricultural sustainability by improving crop yield, nutrient uptake and reducing nitrogen leaching losses. J Appl Ecol. 2015;52:228–239.

Rodriguez A, Sanders IR. The role of community and population ecology in applying mycorrhizal fungi for improved food security. ISME Journal. 2015;9:1053–1061. PubMed PMC

Oviatt P, Rillig MC. Mycorrhizal technologies for an agriculture of the middle. Plants People Planet. 2020:ppp3.10177. doi: 10.1002/ppp3.10177. DOI

Ryan MH, Graham JH. Little evidence that farmers should consider abundance or diversity of arbuscular mycorrhizal fungi when managing crops. New Phytologist. 2018;220:1092–1107. PubMed

Rillig MC, et al. Why farmers should manage the arbuscular mycorrhizal symbiosis. New Phytol. 2019;222:1171–1175. PubMed

Zhang S, Lehmann A, Zheng W, You Z, Rillig MC. Arbuscular mycorrhizal fungi increase grain yields: a meta-analysis. New Phytol. 2019;222:543–555. PubMed

Thirkell TJ, Charters MD, Elliott AJ, Sait SM, Field KJ. Are mycorrhizal fungi our sustainable saviours? Considerations for achieving food security. J Ecol. 2017;105:921–929.

Davison J, et al. Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science (80-.) 2015;349:970–973. PubMed

Pringle A, Bever JD. Analogous effects of arbuscular mycorrhizal fungi in the laboratory and a North Carolina field. New Phytol. 2008;180:162–175. PubMed

Francis R, Read DJ. Mutualism and antagonism in the mycorrhizal symbiosis, with special reference to impacts on plant community structure. Can J Bot. 1995;73:1301–1309.

Thirkell TJ, Pastok D, Field KJ. Carbon for nutrient exchange between arbuscular mycorrhizal fungi and wheat varies according to cultivar and changes in atmospheric carbon dioxide concentration. Glob Chang Biol. 2020;26:1725–1738. PubMed PMC

Lehmann A, Barto EK, Powell JR, Rillig MC. Mycorrhizal responsiveness trends in annual crop plants and their wild relatives—a meta-analysis on studies from 1981 to 2010. Plant Soil. 2012;355:231–250.

Martín-Robles N, et al. Impacts of domestication on the arbuscular mycorrhizal symbiosis of 27 crop species. New Phytol. 2018;218:322–334. PubMed

Leake J, et al. Networks of power and influence: The role of mycorrhizal mycelium in controlling plant communities and agroecosystem functioning. Can J Bot. 2004;82:1016–1045.

Oehl F, et al. Impact of Land Use Intensity on the Species Diversity of Arbuscular Mycorrhizal Fungi in Agroecosystems of Central Europe. Appl Environ Microbiol. 2003;69:2816–2824. PubMed PMC

Xiang D, et al. Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytol. 2014;204:968–978. PubMed

Bainard LD, et al. Plant communities and soil properties mediate agricultural land use impacts on arbuscular mycorrhizal fungi in the Mixed Prairie ecoregion of the North American Great Plains. Agric Ecosyst Environ. 2017;249:187–195.

Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW. Ploughing up the wood-wide web? Nature. 1998;394:431. PubMed

van der Heijden MGA, et al. Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature. 1998;396:69–72.

Vogelsang KM, Reynolds HL, Bever JD. Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol. 2006;172:554–562. PubMed

Scheublin TR, Ridgway KP, Young JPW, van der Heijden MGA. Nonlegumes, Legumes, and Root Nodules Harbor Different Arbuscular Mycorrhizal Fungal Communities. Appl Environ Microbiol. 2004;70:6240–6246. PubMed PMC

Oehl F, et al. Soil type and land use intensity determine the composition of arbuscular mycorrhizal fungal communities. Soil Biol Biochem. 2010;42:724–738.

De Vries FT, et al. Soil food web properties explain ecosystem services across European land use systems. Proc Natl Acad Sci U S A. 2013;110:14296–14301. PubMed PMC

Verbruggen E, Xiang D, Chen B, Xu T, Rillig MC. Mycorrhizal fungi associated with high soil N:P ratios are more likely to be lost upon conversion from grasslands to arable agriculture. Soil Biol Biochem. 2015;86:1–4.

Balami S, Vašutová M, Godbold D, Kotas P, Cudlín P. Soil fungal communities across land use types. IForest. 2020;13:548–558.

Öpik M, Mari M, Liira J, Zobel M. Composition of root-colonizing arbuscular mycorrhizal fungal communities in different ecosystems around the globe. J Ecol. 2006;94:778–790.

Jansa J, et al. Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza. 2002;12:225–234. PubMed

van Groenigen KJ, et al. Abundance, production and stabilization of microbial biomass under conventional and reduced tillage. Soil Biol Biochem. 2010;42:48–55.

Sallach JB, Thirkell TJ, Field KJ, Carter LJ. The emerging threat of human-use antifungals in sustainable and circular agriculture schemes. PLANTS, PEOPLE, PLANET. 2021;3:685–693.

Meyer A, et al. Different Land Use Intensities in Grassland Ecosystems Drive Ecology of Microbial Communities Involved in Nitrogen Turnover in Soil. PLoS One. 2013;8:e73536. PubMed PMC

Tsiafouli MA, et al. Intensive agriculture reduces soil biodiversity across Europe. Glob Chang Biol. 2015;21:973–985. PubMed

Tardy V, et al. Shifts in microbial diversity through land use intensity as drivers of carbon mineralization in soil. Soil Biol Biochem. 2015;90:204–213.

Sawers RJH, et al. Phosphorus acquisition efficiency in arbuscular mycorrhizal maize is correlated with the abundance of root-external hyphae and the accumulation of transcripts encoding PHT1 phosphate transporters. New Phytol. 2017;214:632–643. PubMed

Svenningsen NB, et al. Suppression of the activity of arbuscular mycorrhizal fungi by the soil microbiota. ISME J. 2018;12:1296–1307. PubMed PMC

Schweiger PF, Thingstrup I, Jakobsen I. Comparison of two test systems for measuring plant phosphorus uptake via arbuscular mycorrhizal fungi. Mycorrhiza. 1999;8:207–213.

Emmett BD, Lévesque-Tremblay V, Harrison MJ. Conserved and reproducible bacterial communities associate with extraradical hyphae of arbuscular mycorrhizal fungi. ISME J. 2021;15:2276–2288. PubMed PMC

Jiang F, Zhang L, Zhou J, George TS, Feng G. Arbuscular mycorrhizal fungi enhance mineralisation of organic phosphorus by carrying bacteria along their extraradical hyphae. New Phytol. 2021;230:304–315. PubMed

Thonar C, Schnepf A, Frossard E, Roose T, Jansa J. Traits related to differences in function among three arbuscular mycorrhizal fungi. Plant Soil. 2011;339:231–245.

Cavagnaro TR, Smith FA, Smith SE, Jakobsen I. Functional diversity in arbuscular mycorrhizas: exploitation of soil patches with different phosphate enrichment differs among fungal species. Plant, Cell and Environment. 2005;28

Jakobsen I, Gazey C, Abbott LK. Phosphate transport by communities of arbuscular mycorrhizal fungi in intact soil cores. New Phytol. 2001;149:95–103. PubMed

Pearson JN, Jakobsen I. The relative contribution of hyphae and roots to phosphorus uptake by arbuscular mycorrhizal plants, measured by dual labelling with 32P and 33P. New Phytol. 1993;124:489–494.

Nagy R, Drissner D, Amrhein N, Jakobsen I, Bucher M. Erratum: Mycorrhizal phosphate uptake pathway in tomato is phosphorusrepressible and transcriptionally regulated (New Phytologist (2009) 181 (950-959)) New Phytol. 2009;184:1029 PubMed

Smith SE, Jakobsen I, Grønlund M, Smith FA. Roles of arbuscular mycorrhizas in plant phosphorus nutrition: Interactions between pathways of phosphorus uptake in arbuscular mycorrhizal roots have important implications for understanding and manipulating plant phosphorus acquisition. Plant Physiol. 2011;156:1050–1057. PubMed PMC

Williams A, Manoharan L, Rosenstock NP, Olsson PA, Hedlund K. Long-term agricultural fertilization alters arbuscular mycorrhizal fungal community composition and barley (Hordeum vulgare) mycorrhizal carbon and phosphorus exchange. New Phytol. 2017;213:874–885. PubMed

Koerselman W, Meuleman AFM. The Vegetation N:P Ratio: a New Tool to Detect the Nature of Nutrient Limitation. J Appl Ecol. 1996;33:1441.

Van Aarle IM, Olsson PA, Söderström B. Arbuscular mycorrhizal fungi respond to the substrate pH of their extraradical mycelium by altered growth and root colonization. New Phytol. 2002;155:173–182. PubMed

Staddon PL, et al. Mycorrhizal fungal abundance is affected by long-term climatic manipulations in the field. Glob Chang Biol. 2003;9:186–194.

Weber SE, et al. Responses of arbuscular mycorrhizal fungi to multiple coinciding global change drivers. Fungal Ecol. 2019;40:62–71.

Peat HJ, Fitter AH. The distribution of arbuscular mycorrhizas in the British flora. New Phytol. 1993;125:845–854. PubMed

Cruz-Paredes C, et al. Suppression of arbuscular mycorrhizal fungal activity in a diverse collection of non-cultivated soils. FEMS Microbiol Ecol. 2019;95 PubMed

Jansa J, Erb A, Oberholzer H-R, Šmilauer P, Egli S. Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Mol Ecol. 2014;23:2118–2135. PubMed

Davison J, et al. Temperature and pH define the realised niche space of arbuscular mycorrhizal fungi. New Phytol. 2021;231:763–776. PubMed

Yang H, et al. Changes in soil organic carbon, total nitrogen, and abundance of arbuscular mycorrhizal fungi along a large-scale aridity gradient. Catena. 2011;87:70–77.

Riedo J, et al. Widespread Occurrence of Pesticides in Organically Managed Agricultural Soils—the Ghost of a Conventional Agricultural Past? Environ Sci Technol. 2021 doi: 10.1021/acs.est.0c06405. PubMed DOI

Pánková H, Dostálek T, Vazačová K, Münzbergová Z. Slow recovery of arbuscular mycorrhizal fungi and plant community after fungicide application: An eight-year experiment. J Veg Sci. 2018;29:695–703.

Ipsilantis I, Samourelis C, Karpouzas DG. The impact of biological pesticides on arbuscular mycorrhizal fungi. Soil Biol Biochem. 2012 doi: 10.1016/j.soilbio.2011.08.007. DOI

Buysens C, Dupré de Boulois H, Declerck S. Do fungicides used to control Rhizoctonia solani impact the non-target arbuscular mycorrhizal fungus Rhizophagus irregularis? Mycorrhiza. 2015 doi: 10.1007/s00572-014-0610-7. PubMed DOI

Lekberg Y, Wagner V, Rummel A, McLeod M, Ramsey PW. Strong indirect herbicide effects on mycorrhizal associations through plant community shifts and secondary invasions. Ecol Appl. 2017;27:2359–2368. PubMed

Hage-Ahmed K, Rosner K, Steinkellner S. Arbuscular mycorrhizal fungi and their response to pesticides. Pest Management Science. 2019;75:583–590. PubMed PMC

Kjøller R, Rosendahl S. Effects of fungicides on arbuscular mycorrhizal fungi: differential responses in alkaline phosphatase activity of external and internal hyphae. Biol Fertil Soils. 2000;31:361–365.

Gange AC, Brown VK, Sinclair GS. Vesicular-Arbuscular Mycorrhizal Fungi: A Determinant of Plant Community Structure in Early Succession. Funct Ecol. 1993;7:616.

Hartnett DC, Wilson GWT. The role of mycorrhizas in plant community structure and dynamics: Lessons from grasslands. Plant Soil. 2002;244:319–331.

Guzman A, et al. Crop diversity enriches arbuscular mycorrhizal fungal communities in an intensive agricultural landscape. 2021 doi: 10.1111/nph.17306. PubMed DOI PMC

Eurostat. LUCAS 2018 Technical reference document C3 Classification (Land cover & Land use) 2018;2018:98.

Fick SE, Hijmans RJ. WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. Int J Climatol. 2017;37:4302–4315.

Trabucco A, Zomer R. Global Aridity Index and Potential Evapotranspiration (ET0) Climate Database v2. figshare. 2019 doi: 10.6084/m9.figshare.7504448.v3. PubMed DOI PMC

García-Palacios P, Gross N, Gaitán J, Maestre FT. Climate mediates the biodiversity-ecosystem stability relationship globally. Proc Natl Acad Sci U S A. 2018;115:8400–8405. PubMed PMC

Berdugo M, et al. Global ecosystem thresholds driven by aridity. Science (80-.) 2020;367:787–790. PubMed

Sinnott RW. Virtues of the Haversine. Sky Telescope. 1984;68(2):158.

Garland G, et al. Crop cover is more important than rotational diversity for soil multifunctionality and cereal yields in European cropping systems. Nat Food. 2021;2:28–37. PubMed

Swiss federal research stations. Schweizerische Referenzmethoden der Eidgenössischen Forschungsanstalten. Boden-und Substratuntersuchungen zur Düngeberatung. 1996

Berry D, Ben Mahfoudh K, Wagner M, Loy A. Barcoded Primers Used in Multiplex Amplicon Pyrosequencing Bias Amplification † ‘Barcode-tagged’ PCR primers used for multiplex amplicon sequencing generate a thus-far-overlooked amplification bias that produces variable terminal restriction fragment length polymorphism (T-RFLP) and pyrosequencing data from the same environmental DNA template. We propose a simple two-step PCR ap-proach that increases reproducibility and consistently recovers higher genetic diversity in pyrosequencing libraries. Appl Environ Microbiol. 2011;77:7846–7849. PubMed PMC

Gardes M, White TJ, Fortin JA, Bruns TD, Taylor JW. Identification of indigenous and introduced symbiotic fungi in ectomycorrhizae by amplification of nuclear and mitochondrial ribosomal DNA. Can J Bot. 1991;69:180–190.

Gardes M, Bruns TD. ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Mol Ecol. 1993;2:113–118. PubMed

Fiore-Donno AM, et al. New barcoded primers for efficient retrieval of cercozoan sequences in high-throughput environmental diversity surveys, with emphasis on worldwide biological soil crusts. Mol Ecol Resour. 2018;18:229–239. PubMed

Helfenstein J, Jegminat J, McLaren TI, Frossard E. Soil solution phosphorus turnover: Derivation, interpretation, and insights from a global compilation of isotope exchange kinetic studies. Biogeosciences. 2018;15:105–114.

Thirkell TJ, et al. Cultivar-dependent increases in mycorrhizal nutrient acquisition by barley in response to elevated CO 2. PLANTS, PEOPLE, PLANET. 2021;3:553–566.

Rodushkin I, Ruth T, Huhtasaari Å. Comparison of two digestion methods for elemental determinations in plant material by ICP techniques. Anal Chim Acta. 1999;378:191–200.

Ohno T, Zibilske LM. Determination of Low Concentrations of Phosphorus in Soil Extracts Using Malachite Green. Soil Sci Soc Am J. 1991;55:892–895.

Frossard E, et al. The Use of Tracers to Investigate Phosphate Cycling in Soil–Plant Systems. 2011:59–91. doi: 10.1007/978-3-642-15271-9_3. DOI

Sato K, Suyama Y, Saito M, Sugawara K. A new primer for discrimination of arbuscular mycorrhizal fungi with polymerase chain reaction-denature gradient gel electrophoresis. Grassl Sci. 2005;51:179–181.

Callahan BJ, et al. DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016;13:581–583. PubMed PMC

Bolyen E, et al. Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nat Biotechnol. 2019;37:852–857. PubMed PMC

Öpik M, et al. The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota) New Phytol. 2010;188:223–241. PubMed

Rognes T, Flouri T, Nichols B, Quince C, Mahé F. VSEARCH: a versatile open source tool for metagenomics. PeerJ. 2016;4:e2584. PubMed PMC

Quast C, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2012;41:D590–D596. PubMed PMC

McMurdie PJ, Holmes S. phyloseq: An R Package for Reproducible Interactive Analysis and Graphics of Microbiome Census Data. PLoS One. 2013;8:e61217. PubMed PMC

R Core team. R: A Language and Environment for Statistical Computing. 2013

Calcagno V. Model Selection and Multimodel Inference Made Easy [R package glmulti version 1.0.8] 2020

Cade BS. Model averaging and muddled multimodel inferences. Ecology. 2015 doi: 10.1890/14-1639.1. PubMed DOI

Barton K. MuMIn: Multi-Model Inference R package version 1.43.17. Version 1. 2020:18.

Model Selection and Multimodel Inference. Springer; New York: 2002. DOI

Rosseel Y. Lavaan: An R package for structural equation modeling. J Stat Softw. 2012 doi: 10.18637/jss.v048.i02. DOI

Zobrazit více v PubMed

figshare
10.6084/m9.figshare.15134328, 10.6084/m9.figshare.15134670