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Arbuscular mycorrhizal fungal communities of forbs and C3 grasses respond differently to cultivation and elevated nutrients

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Abstract

Arbuscular mycorrhizal fungi (AMF) represent important players in the structure and function of many ecosystems. Yet, we learn about their roles mostly from greenhouse-based experiments, with results subjected to cultivation bias. This study explores multiple aspects of this bias and separates the effect of increased nutrient availability from other cultivation specifics. For 15 grassland plant species from two functional groups (C3 grasses vs dicotyledonous forbs), we compared AMF communities of adults collected from non-manipulated vegetation with those in plants grown in a greenhouse. Nutrient availability was comparable to field conditions or experimentally elevated. We evaluated changes in AMF community composition, diversity, root colonisation, and the averages of functional traits characterising hyphal soil exploration. Additionally, we use the data from the greenhouse experiment to propose a new plant functional trait—the change of AMF colonisation in response to nutrient surplus. The AMF community differed profoundly between field-collected and greenhouse-grown plants, with a larger change of its composition in grass species, and AMF community composition in grasses also responded more to fertilisation than in forbs. Taxonomic and phylogenetic diversity declined more in forbs under cultivation (particularly with elevated nutrients), because in their roots, the AMF taxa from families other than Glomeraceae largely disappeared. A decline in AMF colonisation was not caused by greenhouse cultivation itself but selectively by the elevation of nutrient availability, particularly in grass host species. We demonstrate that the extent of decrease in AMF colonisation with elevated nutrients is a useful plant functional trait explaining an observed response of the plant community to manipulation.

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Availability of data and material

DNA sequences: GenBank accessions MW629950-MW630040, see SI Table S2. Quality-controlled results of NGS and light microscopy, as well as the explanatory variables will be accessible on zenodo.org platform from the January 2022 (Šmilauer et al. 2021).

References 

  • Anslan S, Bahram M, Hiiesalu I, Tedersoo L (2017) PipeCraft: flexible open-source toolkit for bioinformatics analysis of custom high-throughput amplicon sequencing data. Mol Ecol Resour 17:e234–e240

    Article  CAS  PubMed  Google Scholar 

  • Antunes PM, Lehmann A, Hart MM, Baumecker M, Rillig MC (2012) Long-term effects of soil nutrient deficiency on arbuscular mycorrhizal communities. Funct Ecol 26:532–540

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effect models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Bennett JA, Cahill JF (2016) Fungal effects on plant-plant interactions contribute to grassland plant abundances: evidence from the field. J Ecol 104:755–764

    Article  Google Scholar 

  • Chen ECH, Morin E, Beaudet D, Noel J, Yildirir G, Ndikumana S et al (2018) High intraspecific genome diversity in the model arbuscular mycorrhizal symbiont Rhizophagus irregularis. New Phytol 220:1161–1171

    Article  CAS  PubMed  Google Scholar 

  • Chung YA, Jumpponen A, Rudgets JA (2019) Divergence in diversity and composition of root-associated fungi between greenhouse and field studies in a semiarid grassland. Microb Ecol 78:122–135

    Article  PubMed  Google Scholar 

  • Davison J, de León DG, Zobel M, Moora M, Bueno CG, Barceló M et al (2020) Plant functional groups associate with distinct arbuscular mycorrhizal fungal communities. New Phytol 226:1117–1128

    Article  PubMed  Google Scholar 

  • de Kroon H, Mommer L (2006) Root foraging theory put to the test. Trends Ecol Evol 21:113–116

    Article  PubMed  Google Scholar 

  • Delavaux CS, Smith-Ramesh LM, Kuebbing SE (2017) Beyond nutrients: a meta-analysis of the diverse effects of arbuscular mycorrhizal fungi on plants and soils. Ecology 98:2111–2119

    Article  PubMed  Google Scholar 

  • Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochemical Bulletin 19:11–15

    Google Scholar 

  • Dumbrell AJ, Ashton PD, Aziz N, Feng G, Nelson M, Dytham C, Fitter AH, Helgasson T (2011) Distinct seasonal assemblages of arbuscular mycorrhizal fungi revealed by massively parallel pyrosequencing. New Phytol 190:794–804

    Article  CAS  PubMed  Google Scholar 

  • Egan CP, Rummel A, Kokkoris V, Klironomos J, Lekberg Y, Hart M (2018) Using mock communities of arbuscular mycorrhizal fungi to evaluate fidelity associated with Illumina sequencing. Fungal Ecol 33:52–64

    Article  Google Scholar 

  • Egerton-Warburton LM, Johnson NC, Allen EB (2007) Mycorrhizal community dynamics following nitrogen fertilization: a cross-site test in five grasslands. Ecol Monogr 77:527–544

    Article  Google Scholar 

  • Fay PA, Prober SM, Harpole WS, Knops JMH, Bakker JD, Borer ET et al (2015) Grassland productivity limited by multiple nutrients. Nature Plants 1:15080

    Article  CAS  PubMed  Google Scholar 

  • Field KJ, Bidartondo MI, Rimington WR, Hoysted GA, Beerling DJ, Cameron DD et al (2019) Functional complementarity of ancient plant-fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts. New Phytol 223:908–921

    Article  CAS  PubMed  Google Scholar 

  • Guerrero-Ramírez NR, Mommer L, Freschet GT, Iversen CM, McCormack ML, Kattge J, Poorter H, Weigelt A (2021) Global root traits (GRooT) database. Glob Ecol Biogeogr 30:25–37

    Article  Google Scholar 

  • Guindon S, Dufavard JF, Lefort V, Anisimova M, Hordijk W, Gascuel O (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321

    Article  CAS  PubMed  Google Scholar 

  • Henning JA, Weiher E, Lee TD, Freund D, Stefanski A, Bentivenga SP (2018) Mycorrhizal fungal spore community structure in a manipulated prairie. Restor Ecol 26:124–133

    Article  Google Scholar 

  • Janos DP (2007) Plant responsiveness to mycorrhizas differs from dependence upon mycorrhizas. Mycorrhiza 17:75–91

    Article  PubMed  Google Scholar 

  • Jansa J, Mozafar A, Frossard E (2005) Phosphorus acquisition strategies within arbuscular mycorrhizal community of a single field site. Plant Soil 276:163–176

    Article  CAS  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. Mol Ecol 23:2118–2135

    Article  CAS  PubMed  Google Scholar 

  • Jiang S, Liu Y, Luo J, Qin M, Johnson NC, Öpik M et al (2018) Dynamics of arbuscular mycorrhizal fungal community structure and functioning along a nitrogen enrichment gradient in an alpine meadow ecosystem. New Phytol 220:1222–1235

    Article  PubMed  Google Scholar 

  • Johnson NC, Rowland DL, Corkidi L, Allen EB (2008) Plant winners and losers during grassland N-eutrophication differ in biomass allocation and mycorrhizas. Ecology 89:2868–2878

    Article  PubMed  Google Scholar 

  • Kaplan Z, Danihelka J, Chrtek jun J, Kirschner J, Kubát K, Štech M, Štěpánek J (2019) Key to the Flora of the Czech Republic [in Czech], 2nd edn. Academia, Praha, p 1168

    Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kim H, Heo E, Kang H, Adams J (2013) Changes in soil bacterial community structure with increasing disturbance frequency. Microb Ecol 66:171–181

    Article  PubMed  Google Scholar 

  • Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M et al (2008) The LEDA Traitbase: A database of life-history traits of Northwest European flora. J Ecol 96:1266–1274

    Article  Google Scholar 

  • Klimešová J, Danihelka J, Chrtek J, de Bello F, Herben T (2017) CLO-PLA: a database of clonal and bud-bank traits of the Central European flora. Ecology 98:1179

    Article  PubMed  Google Scholar 

  • Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65:339–349

    Article  CAS  PubMed  Google Scholar 

  • Legendre P, Legendre L (2012) Numerical Ecology. Third English Edition. Elsevier, Amsterdam. 990 pp

  • Lin G, McCormack ML, Guo D (2015) Arbuscular mycorrhizal fungal effects on plant competition and community structure. J Ecol 103:1224–1232

    Article  CAS  Google Scholar 

  • Liu Y, Johnson NC, Mao L, Shi G, Jiang S, Ma X et al (2015) Phylogenetic structure of arbuscular mycorrhizal community shifts in response to increasing soil fertility. Soil Biol Biochem 89:196–205

    Article  CAS  Google Scholar 

  • Middleton EL, Richardson S, Koziol L, Palmer CE, Yermakov Z, Henning JA et al (2015) Locally adapted arbuscular mycorrhizal fungi improve vigor and resistance to herbivory of native prairie plant species. Ecosphere 6:article 276

  • Ohsowski BM, Zaitsoff PD, Öpik M, Hart MM (2014) Where the wild things are: looking for uncultured Glomeromycota. New Phytol 204:171–179

    Article  PubMed  Google Scholar 

  • Orchard S, Standish RJ, Dickie IA, Renton M, Walker C, Moot D, Ryan MH (2017) Fine root endophytes under scrutiny: a review of the literature on arbuscule-producing fungi recently suggested to belong to the Mucoromycotina. Mycorhiza 27:619–638

    Article  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/

  • Schloss PD, Westcott SL, Ryabin T, Hall JR, Hartmann M, Hollister EB et al (2009) Introducing Mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl Environ Microbiol 75:7537–7541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Šmilauer P, Košnar J, Kotilínek M, Šmilauerová M (2020a) Contrasting effects of host identity, plant community, and local species pool on the composition and colonization levels of arbuscular mycorrhizal fungal community in a temperate grassland. New Phytol 225:461–473

    Article  PubMed  Google Scholar 

  • Šmilauer P, Šmilauerová M, Kotilínek M, Košnar J (2020b) Foraging speed and precision of arbuscular mycorrhizal fungi under field conditions: an experimental approach. Mol Ecol 29:1574–1587

    Article  PubMed  Google Scholar 

  • Šmilauer P, Šmilauerová M, Kotilínek M, Košnar J (2021) Arbuscular mycorrhizal fungal communities of forbs and C3 grasses respond differently to cultivation and elevated nutrients . Public repository zenodo.org, https://doi.org/10.5281/zenodo.4736394

  • Sýkorová Z, Ineichen K, Wiemken A, Redecker D (2007) The cultivation bias: different communities of arbuscular mycorrhizal fungi detected in roots from the field, from bait plant transplanted to the field, and from a greenhouse trap experiment. Mycorrhiza 18:1–14

    Article  PubMed  Google Scholar 

  • Ter Braak CJF, Šmilauer P (2018) Canoco reference manual and user’s guide: software for ordination (version 5.10). Microcomputer Power, Ithaca. 536 pp

  • Treseder KK, Allen EB, Egerton-Warburton LM, Hart MM, Klironomos JN, Maherali H, Tedersoo L (2018) Arbuscular mycorrhizal fungi as mediators of ecosystem responses to nitrogen deposition: a trait-based predictive framework. J Ecol 106:480–489

    Article  CAS  Google Scholar 

  • Unger S, Friede M, Hundacker J, Volkmar K, Beyschlag W (2016) Allocation trade-off between root and mycorrhizal surface defines nitrogen and phosphorus relations in 13 grassland species. Plant Soil 407:279–291

    Article  CAS  Google Scholar 

  • Van der Heijden MGA, Martin FM, Sellose MA, Sanders IR (2018) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205:1406–1423

    Article  Google Scholar 

  • Vasar M, Andreson R, Davison J, Jairus T, Moora M, Remm M et al (2017) Increased sequencing depth does not increase captured diversity of arbuscular mycorrhizal fungi. Mycorrhiza 27:761–773

    Article  CAS  PubMed  Google Scholar 

  • Větrovský T, Baldrian P, Morais D (2018) SEED 2: a user-friendly platform for amplicon high-throughput sequencing data analyses. Bioinformatics 34:2292–2294

    Article  PubMed  PubMed Central  Google Scholar 

  • Vierheilig H, Schweiger P, Brundrett M (2005) An overview of methods for the detection and observation of arbuscular mycorrhizal fungi in roots. Physiol Plant 125:393–404

    CAS  Google Scholar 

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Acknowledgements

All authors thank Blanka Divišová for all her work in the laboratory; MS wishes to thank God for the overall support of her work. Authors are also thankful to reviewers and the manuscript editor for their careful reading and many good suggestions.

Funding

This research was financially aided by a grant from the Czech Science Foundation (GACR 17-10878S).

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P. Šmilauer and M. Šmilauerová designed the experiment and collected data; J. Košnar and M. Kotilínek optimised and performed molecular and bioinformatic analyses; P. Šmilauer analysed data; P. Šmilauer and J. Košnar wrote the text; and all authors contributed to its further improvement.

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Correspondence to Petr Šmilauer.

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Šmilauer, P., Šmilauerová, M., Kotilínek, M. et al. Arbuscular mycorrhizal fungal communities of forbs and C3 grasses respond differently to cultivation and elevated nutrients. Mycorrhiza 31, 455–470 (2021). https://doi.org/10.1007/s00572-021-01036-3

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