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Geography and habitat predominate over climate influences on arbuscular mycorrhizal fungal communities of mid-European meadows

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Abstract

Despite the crucial importance of arbuscular mycorrhizal fungi (AMF) for numerous processes within terrestrial ecosystems, knowledge of the determinants of AMF community structure still is limited, mainly because of the limited scope of the available individual case studies which often only include a few environmental variables. Here, we describe the AMF diversity of mid-European meadows (mown or regularly cut grasslands, or recently abandoned lands where grasslands established spontaneously) within a considerably heterogeneous landscape over a scale of several hundred kilometers with regard to macroclimatic, microclimatic, and soil parameters. We include data describing the habitat (including vegetation type), geography, and climate, and test their contribution to the structure of the AMF communities at a regional scale. We amplified and sequenced the ITS 2 region of the ribosomal DNA operon of the AMF from soil samples using nested PCR and Illumina pair-end amplicon sequencing. Habitat (especially soil pH) and geographical parameters (spatial distance, altitude, and longitude) were the main determinants of the structure of the AMF communities in the meadows at a regional scale, with the abundance of genera Septoglomus, Paraglomus, Archaeospora, Funneliformis, and Dominikia driving the main response. The effects of climate and vegetation type were not significant and were mainly encompassed within the geography and/or soil pH effects. This study illustrates how important it is to have a large set of environmental metadata to compare the importance of different factors influencing the AMF community structure at large spatial scales.

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References

  • Allen MF (2007) Mycorrhizal fungi: highways for water and nutrients in arid soils. Vadose Zone J 6:291–297

    Google Scholar 

  • Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses. New Phytol 173:808–816

    CAS  PubMed  Google Scholar 

  • Augé RM, Toler HD, Saxton AM (2014) Arbuscular mycorrhizal symbiosis and osmotic adjustment in response to NaCl stress: a meta-analysis. Front Plant Sci 5:562

    PubMed  PubMed Central  Google Scholar 

  • Augé RM, Toler HD, Saxton AM (2015) Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis. Mycorrhiza 25:13–24

    PubMed  Google Scholar 

  • Baas-Becking LGM (1934) Geobiologie of Inleiding Tot de Milieukunde. Van Stockkum und Zoon, The Hague

    Google Scholar 

  • Barnes CJ, van der Gast CJ, Burns CA, McNamara NP, Bending GD (2016) Temporally variable geographical distance effects contribute to the assembly of root-associated fungal communities. Front Microbiol 7:196

    Google Scholar 

  • Bever JD, Dickie IA, Facelli E, Facelli JM, Klironomos J, Moora M, Rillig MC, Stock WD, Tibbett M, Zobel M (2010) Rooting theories of plant community ecology in microbial interactions. Trends Ecol Evol 25:468–478

    PubMed  PubMed Central  Google Scholar 

  • Boeraeve M, Honnay O, Jacquemyn H (2019) Local abiotic conditions are more important than landscape context for structuring arbuscular mycorrhizal fungal communities in the roots of a forest herb. Oecologia. 190:149–157. https://doi.org/10.1007/s00442-019-04406-z

    Article  PubMed  Google Scholar 

  • Bonfim JA, Vasconcellos RLF, Gumiere T, Mescolotti DDLC, Oehl F, Cardoso EJBN (2016) Diversity of arbuscular mycorrhizal fungi in a Brazilian Atlantic forest toposequence. Microb Ecol 71:164–177

    PubMed  Google Scholar 

  • Bruns TD, Corradi N, Redecker D, Taylor JW, Öpik M (2017) Glomeromycotina: what is a species and why should we care? New Phytol. https://doi.org/10.1111/nph.14913

    Google Scholar 

  • Cao HC, Chen RR, Wang LB, Jiang LL, Yang F, Zheng SX, Wang GJ, Lin XG (2016) Soil pH, total phosphorus, climate and distance are the major factors influencing microbial activity at a regional spatial scale. Sci Rep 6:10

    Google Scholar 

  • Chytrý M (2007) Vegetation of the Czech Republic. Academia, Prague

    Google Scholar 

  • Chytrý M (2009) Vegetation of the Czech Republic. Academia, Prague

    Google Scholar 

  • Chytrý M (2011) Vegetation of the Czech Republic. Academia, Prague

    Google Scholar 

  • Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Ba A, Burla S, Diedhiou AG, Hiiesalu I, Jairus T, Johnson NC, Kane A, Koorem K, Kochar M, Ndiaye C, Partel M, Reier U, Saks U, Singh R, Vasar M, Zobel M (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349:970–973

    CAS  PubMed  Google Scholar 

  • Dray S, Pelissier R, Couteron P, Fortin MJ, Legendre P, Peres-Neto PR, Bellier E, Bivand R, Blanchet FG, de Caceres M, Dufour AB, Heegaard E, Jombart T, Munoz F, Oksanen J, Thioulouse J, Wagner HH (2012) Community ecology in the age of multivariate multiscale spatial analysis. Ecol Monogr 82:257–275

    Google Scholar 

  • Dumbrell AJ, Nelson M, Helgason T, Dytham C, Fitter AH (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4:1078–1078

    Google Scholar 

  • Evelin H, Kapoor R, Giri B (2009) Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot 104:1263–1280

    CAS  PubMed  PubMed Central  Google Scholar 

  • Federhen S (2012) The NCBI taxonomy database. Nucleic Acids Res 40:D136–D143

    CAS  PubMed  Google Scholar 

  • Hazard C, Gosling P, van der Gast CJ, Mitchell DT, Doohan FM, Bending GD (2013) The role of local environment and geographical distance in determining community composition of arbuscular mycorrhizal fungi at the landscape scale. ISME J 7:498–508

    CAS  PubMed  Google Scholar 

  • Hijri I, Sýkorová Z, Oehl F, Ineichen K, Mäder P, Wiemken A, Redecker D (2006) Communities of arbuscular mycorrhizal fungi in arable soils are not necessarily low in diversity. Molec Ecol 15:2277–2289

    CAS  Google Scholar 

  • Husband R, Herre EA, Turner SL, Gallery R, Young JPW (2002) Molecular diversity of arbuscular mycorrhizal fungi and patterns of host association over time and space in a tropical forest. Molec Ecol 11:2669–2678

    CAS  Google Scholar 

  • Jansa J, Mozafar A, Anken T, Ruh R, Sanders IR, Frossard E (2002) Diversity and structure of AMF communities as affected by tillage in a temperate soil. Mycorrhiza 12:225–234

    CAS  PubMed  Google Scholar 

  • Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176

    Google Scholar 

  • Jansa J, Erb A, Oberholzer HR, Šmilauer P, Egli S (2014) Soil and geography are more important determinants of indigenous arbuscular mycorrhizal communities than management practices in Swiss agricultural soils. Molec Ecol 23:2118–2135

    CAS  Google Scholar 

  • Jansa J, Řezáčová V, Šmilauer P, Oberholzer HR, Egli S (2016) Root colonization of bait plants by indigenous arbuscular mycorrhizal fungal communities is not a suitable indicator of agricultural land-use legacy. Agri Ecos Environ 231:310–319

    Google Scholar 

  • Johnson D, Martin F, Cairney JWG, Anderson IC (2012) The importance of individuals: intraspecific diversity of mycorrhizal plants and fungi in ecosystems. New Phytol 194:614–628

    PubMed  Google Scholar 

  • Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43:2294–2303

    CAS  Google Scholar 

  • Konvalinková T, Püschel D, Řezáčová V, Gryndlerová H, Jansa J (2017) Carbon flow from plant to arbuscular mycorrhizal fungi is reduced under phosphorus fertilization. Plant Soil 419:319–333

    Google Scholar 

  • Krüger M, Stockinger H, Krüger C, Schüssler A (2009) DNA-based species level detection of Glomeromycota: one PCR primer set for all arbuscular mycorrhizal fungi. New Phytol 183:212-23

    Google Scholar 

  • Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molec Biol Evol 35:1547–1549

    CAS  PubMed  PubMed Central  Google Scholar 

  • Leifheit EF, Veresoglou SD, Lehmann A, Morris EK, Rillig MC (2014) Multiple factors influence the role of arbuscular mycorrhizal fungi in soil aggregation - a meta-analysis. Plant Soil 374:523–537

    CAS  Google Scholar 

  • Lekberg Y, Koide RT, Rohr JR, Aldrich-Wolfe L, Morton JB (2007) Role of niche restrictions and dispersal in the composition of arbuscular mycorrhizal fungal communities. J Ecol 95:95–105

    Google Scholar 

  • Lekberg Y, Hammer EC, Olsson PA (2010) Plants as resource islands and storage units - adopting the mycocentric view of arbuscular mycorrhizal networks. FEMS Microbiol Ecol 74:336–345

    CAS  PubMed  Google Scholar 

  • Martinez TN, Johnson NC (2010) Agricultural management influences propagule densities and functioning of arbuscular mycorrhizas in low- and high-input agroecosystems in arid environments. Appl Soil Ecol 46:300–306

    Google Scholar 

  • Millar NS, Bennett AE (2016) Stressed out symbiotes: hypotheses for the influence of abiotic stress on arbuscular mycorrhizal fungi. Oecologia 182:625–641

    PubMed  PubMed Central  Google Scholar 

  • Moora M, Berger S, Davison J, Öpik M, Bommarco R, Bruelheide H, Kuhn I, Kunin WE, Metsis M, Rortais A, Vanatoa A, Vanatoa E, Stout JC, Truusa M, Westphal C, Zobel M, Walther GR (2011) Alien plants associate with widespread generalist arbuscular mycorrhizal fungal taxa: evidence from a continental-scale study using massively parallel 454 sequencing. J Biogeogr 38:1305–1317

    Google Scholar 

  • Nei M, Kumar S (2000) Molecular evolution and phylogenetics. Oxford University Press, New York

    Google Scholar 

  • Newsham KK, Fitter AH, Watkinson AR (1995) Arbuscular mycorrhiza protect an annual grass from root pathogenic fungi in the field. J Ecol 83:991–1000

    Google Scholar 

  • Oehl F, Sieverding E, Mäder P, Dubois D, Ineichen K, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583

    PubMed  Google Scholar 

  • Oehl F, Sieverding E, Ineichen K, Mäder P, Wiemken A, Boller T (2009) Distinct sporulation dynamics of arbuscular mycorrhizal fungal communities from different agroecosystems in long-term microcosms. Agri Ecos Environ 134:257–268

    Google Scholar 

  • Oehl F, Laczko E, Oberholzer HR, Jansa J, Egli S (2017) Diversity and biogeography of arbuscular mycorrhizal fungi in agricultural soils. Biol Fertil Soils 53:777–797

    Google Scholar 

  • Ohno T, Zibilske LM (1991) Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci Soc Am J 55:892–895

    CAS  Google Scholar 

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

    Google Scholar 

  • Öpik M, Vanatoa A, Vanatoa E, Moora M, Davison J, Kalwij JM, Reier U, Zobel M (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188:223–241

    PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Rasmussen PU, Hugerth LW, Blanchet FG, Andersson AF, Lindahl BD, Tack AJM (2018) Multiscale patterns and drivers of arbuscular mycorrhizal fungal communities in the roots and root-associated soil of a wild perennial herb. New Phytol 220:1248–1261

    CAS  PubMed  PubMed Central  Google Scholar 

  • Řezáčová V, Gryndler M, Bukovská P, Šmilauer P, Jansa J (2016) Molecular community analysis of arbuscular mycorrhizal fungi - contributions of PCR primer and host plant selectivity to the detected community profiles. Pedobiol 59:179–187

    Google Scholar 

  • Řezáčová V, Slavíková R, Zemková L, Konvalinková T, Procházková V, Šťovíček V, Hršelová H, Beskid O, Hujslová M, Gryndlerová H, Gryndler M, Püschel D, Jansa J (2018) Mycorrhizal symbiosis induces plant carbon reallocation differently in C3 and C4Panicum grasses. Plant Soil 425:441–456

    Google Scholar 

  • Rodríguez-Echeverría S, Teixeira H, Correia M, Timóteo S, Heleno R, Öpik M and Moora M (2017) Arbuscular mycorrhizal fungi communities from tropical Africa reveal strong ecological structure. New Phytol 213: 380–390

    Google Scholar 

  • Smith SE, Smith FA, Jakobsen I (2004) Functional diversity in arbuscular mycorrhizal (AM) symbioses: the contribution of the mycorrhizal P uptake pathway is not correlated with mycorrhizal responses in growth or total P uptake. New Phytol 162:511–524

    Google Scholar 

  • Sochorová L, Jansa J, Verbruggen E, Hejcman M, Schellberg J, Kiers ET, Johnson NC (2016) Long-term agricultural management maximizing hay production can significantly reduce belowground C storage. Agri Ecos Environ 220:104–114

    Google Scholar 

  • Soudzilovskaia NA, Douma JC, Akhmetzhanova AA, van Bodegom PM, Cornwell WK, Moens EJ, Treseder KK, Tibbett M, Wang YP, Cornelissen JHC (2015) Global patterns of plant root colonization intensity by mycorrhizal fungi explained by climate and soil chemistry. Glob Ecol Biogeogr 24:371–382

    Google Scholar 

  • Sousa NMF, Veresoglou SD, Oehl F, Rillig MC, Maia LC (2018) Predictors of arbuscular mycorrhizal fungal communities in the brazilian tropical dry forest. Microbial Ecol 75:447–458

    Google Scholar 

  • Spatafora JW, Chang Y, Benny GL, Lazarus K, Smith ME, Berbee ML, Bonito G, Corradi N, Grigoriev I, Gryganskyi A, James TY, O’Donnell K, Roberson RW, Taylor TN, Uehling J, Vilgalys R, White MM, Stajich JE (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108:1028–1046

    CAS  PubMed  PubMed Central  Google Scholar 

  • ter Braak CJF, Šmilauer P (2018) Canoco reference manual and user’s guide: software for ordination (version 5.10). Biometris, Wageningen University & Research

  • Toljander JF, Eberhardt U, Toljander YK, Paul LR, Taylor AFS (2006) Species composition of an ectomycorrhizal fungal community along a local nutrient gradient in a boreal forest. New Phytol 170:873–883

    CAS  PubMed  Google Scholar 

  • van der Heijden MGA, Klironomos JN, Ursic M, Moutoglis P, Streitwolf-Engel R, Boller T, Wiemken A, Sanders IR (1998) Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396:69–72

    Google Scholar 

  • van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plants. New Phytol 158:601–601

    Google Scholar 

  • van der Heijden MGA, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423

    PubMed  Google Scholar 

  • van Geel M, Ceustermans A, van Hemelrijck W, Lievens B, Honnay O (2015) Decrease in diversity and changes in community composition of arbuscular mycorrhizal fungi in roots of apple trees with increasing orchard management intensity across a regional scale. Molec Ecol 24:941–952

    Google Scholar 

  • van Geel M, Jacquemyn H, Plue J, Saar L, Kasari L, Peeters G, van Acker K, Honnay O, Ceulemans T (2018) Abiotic rather than biotic filtering shapes the arbuscular mycorrhizal fungal communities of European seminatural grasslands. New Phytol 220:1262-1272

  • Verbruggen E, van der Heijden MGA, Weedon JT, Kowalchuk GA, Roling WFM (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Molec Ecol 21:2341–2353

    Google Scholar 

  • Verhoeven KJF, Simonsen KL, McIntyre LM (2005) Implementing false discovery rate control: increasing your power. Oikos 108:643–647

    Google Scholar 

  • Větrovský T, Baldrian P (2013) Analysis of soil fungal communities by amplicon pyrosequencing: current approaches to data analysis and the introduction of the pipeline SEED. Biol Fertil Soils 49:1027–1037

    Google Scholar 

  • Vigo C, Norman JR, Hooker JE (2000) Biocontrol of the pathogen Phytophthora parasitica by arbuscular mycorrhizal fungi is a consequence of effects on infection loci. Plant Pathol 49:509–514

    Google Scholar 

  • White TJ, Bruns TD, Lee SB, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols — a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Xiang D, Verbruggen E, Hu YJ, Veresoglou SD, Rillig MC, Zhou W, Xu TL, Li H, Hao ZP, Chen YL, Chen BD (2014) Land use influences arbuscular mycorrhizal fungal communities in the farming-pastoral ecotone of northern China. New Phytol 204:968–978

    CAS  PubMed  Google Scholar 

  • Xu TL, Veresoglou SD, Chen YL, Rillig MC, Xiang D, Ondrej D, Hao ZP, Liu L, Deng Y, Hu YJ, Chen WP, Wang JT, He JZ, Chen BD (2016) Plant community, geographic distance and abiotic factors play different roles in predicting AMF biogeography at the regional scale in northern China. Environ Microbiol Rep 8:1048–1057

    CAS  PubMed  Google Scholar 

  • Yang HS, Zang YY, Yuan YG, Tang JJ, Chen X (2012) Selectivity by host plants affects the distribution of arbuscular mycorrhizal fungi: evidence from ITS rDNA sequence metadata. BMC Evol Biol 12:50

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

This research was supported by the Czech Science Foundation (Project 18-01486S), the Ministry of Education, Youth and Sports of the Czech Republic (Project LK11224), and the Long-term Development Program RVO 61388971.

Data accessibility

Explanatory variable data are available as a supplement to this article (Online Resource 2). Sequences have been deposited in the Sequence Read Archive (NCBI) under PRJNA 414957/SRP 120469, temporary submission ID: SUB 3139645.

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Authors and Affiliations

  1. Laboratory of Fungal Biology, Institute of Microbiology, Czech Academy of Sciences, Prague, Czech Republic

    Veronika Řezáčová, Renata Slavíková, Tereza Konvalinková, Lenka Zemková, Milan Řezáč, Milan Gryndler, Hana Gryndlerová, Hana Hršelová, Petra Bukovská & Jan Jansa

  2. Biodiversity Lab, Crop Research Institute, Prague, Czech Republic

    Veronika Řezáčová & Milan Řezáč

  3. Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic

    Petr Šmilauer

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  1. Veronika Řezáčová
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Contributions

JJ, TK, MG, and LZ planned the field sample collection strategy. TK and LZ collected the field samples and recorded the details of the vegetation cover at the sampling sites. TK, LZ, VŘ, RS, HH, MŘ, HG, MG, and PB processed the field samples, carried out the analyses, and/or processed the metadata. VŘ and PŠ analyzed the data, and VŘ and JJ wrote the manuscript. All authors approved the final version of the manuscript.

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Correspondence to Veronika Řezáčová.

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Řezáčová, V., Slavíková, R., Konvalinková, T. et al. Geography and habitat predominate over climate influences on arbuscular mycorrhizal fungal communities of mid-European meadows. Mycorrhiza 29, 567–579 (2019). https://doi.org/10.1007/s00572-019-00921-2

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