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Land-use intensity and soil properties shape the composition of fungal communities in Mediterranean peaty soils drained for agricultural purposes

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Abstract

Anthropogenic effects on soil fungi have been poorly investigated in peaty soils, where they have a crucial role in the maintenance of soil fertility and in the regulation of nutrient cycles. In this study, we assessed the effects of land-use intensification on the composition of fungal communities in Mediterranean peaty soils drained for agricultural purposes. To this end, a continuous maize cropping system was compared with an extensive grassland and an agricultural soil left abandoned for 15 years. Molecular diversity and community composition of total soil fungi and arbuscular mycorrhizal fungi (AMF) were assessed, as well as soil chemical properties potentially responsible for fungal shifts. The relative roles of intensification and soil chemical properties were also quantified by applying variation partitioning analysis. Multivariate analyses show that: (i) land-use intensification shapes the composition of the community of total soil fungi and AMF in soil and roots; (ii) base saturation (Bas Sat) and exchangeable calcium (ExchCa) in soil are the significant soil chemical drivers of the composition of the total soil fungal community; (iii) Bas Sat is the only significant chemical parameter shaping the soil AMF community; and (iv) no soil chemical properties affect root AMF. Based on variation partitioning, which highlights a large overlap between land-use intensification and Bas Sat, we can assert that land-use intensification is well-correlated with Bas Sat in shaping the total soil fungal community composition, as well as the AMF. By contrast, intensification acts as a major driver with respect to ExchCa in shaping the composition of the total soil fungal communities.

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Acknowledgments

This work represents part of the PhD thesis project of C.V. which was funded by Scuola Superiore Sant’Anna. The work was also supported by the “Consorzio di Bonifica Versilia-Massaciuccoli” and the “Regione Toscana” (“Restoration of a Mediterranean Drained Peatland”: https://sites.google.com/site/restomedpeat-land/home). We are grateful to Martti Vasar for his bioinformatic advices. The authors wish to thank the two anonymous reviewers and the editor for their help in improving the previous version of the manuscript.

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Authors and Affiliations

  1. Institute of Life Sciences, Sant’Anna School of Advanced Studies, P.za Martiri della Libertà 33, 56127, Pisa, Italy

    Valentina Ciccolini, Enrico Bonari & Elisa Pellegrino

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  1. Valentina Ciccolini
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  2. Enrico Bonari
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  3. Elisa Pellegrino
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Correspondence to Elisa Pellegrino.

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Supplementary Fig. S6

Neighbor-Joining (NJ) tree of total soil fungal sequences derived from soil from three levels of intensification of land use: high intensity (diamond; HI: maize monoculture), low intensity (square; LI: extensive grassland) and zero intensity (triangle; ZI: agricultural soil left abandoned). NJ is based on the fungal 18S rRNA gene (≈ 1650 bp; NS1/FR1 fragment) and involved 143 newly detected nucleotide sequences plus 25 reference sequences retrieved from the NCBI database. The tree is rooted with Meristolohmannia meristacaroides. The sequences retrieved were classified in 16 AMF molecular operational taxonomic units (MOTUs) affiliated with the orders Hypocreales (1, 2), Sordariales (3), Xylariales (4), Chaetothyriales (5), Eurotiales (6), Pleosporales (7), Dothideomycetes (8), Helotiales (9), Agaricales (10), Gomphales (11), Corticiales (12), Filobasidiales (13), Tremellales (14) and to two classes Chytridiomycota (15) and Zygomycota (16). Bootstrap values (based on 1000 replicates) are shown at the nodes. The scale bar indicates substitutions per site. Sequences obtained in the present study are shown in bold, and their accession numbers are prefixed by the internal clone identifier (H) and the soil sample number from which they were obtained. All new sequences were submitted to the EMBL nucleotide sequence database (accession numbers: LN555148 - LN555383 and LN555530 - LN555579) (JPEG 1.37 MB)

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Supplementary Fig. S7

Rarefaction curves showing the relation between sampled sequence number and the number of observed molecular operational taxonomic units (MOTUs) of (a) soil arbuscular mycorrhizal fungi (AMF), (b) root AMF and (c) total soil fungi retrieved in three levels of intensification of land use: high intensity (HI; maize monoculture; red line), low intensity (LI; extensive grassland; yellow line) and zero intensity (ZI; agricultural soil left abandoned; green line). AMF sequences from HI and ZI land-use types are from Pellegrino et al. (2014) (JPEG 162 kb)

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Supplementary Fig. S8

Neighbor-Joining tree of sequences of arbuscular mycorrhizal fungi (AMF) derived from soil and roots (open and filled symbols, respectively) from three levels of intensification of land use: high intensity (diamond; HI: maize monoculture), low intensity (square; LI: extensive grassland) and zero intensity (triangle; ZI: agricultural soil left abandoned). Analysis is based on SSU rRNA gene sequences (SSU ≈ 550 bp; NS31/AM1 fragment) and involved 339 sequences (139 newly detected nucleotide sequences, 160 sequences retrieved from Pellegrino et al. (2014), 27 from the reference dataset, 12 from GenBank). The tree is rooted with Corallochytrium limacisporum. The sequences retrieved were classified in 17 AMF molecular operational taxonomic units (MOTUs) affiliated with Funneliformis sp. (12, 13), Rhizophagus sp. (5, 6, 7), Sclerocystis sp. (4), Scutellospora sp. (15), Glomus spp. (1, 2, 3, 8, 9, 10, 11, 14) and uncultured Glomeromycota (16, 17). Bootstrap values (based on 1000 replicates) are shown at the nodes. The scale bar indicates substitutions per site. Sequences obtained in the present study are shown in bold, and their accession numbers are prefixed by the internal clone identifier (clones from roots and soil are identified by a and G, respectively) and the root/soil sample number from which they were obtained. Sequences from HI and ZI land-use types are from Pellegrino et al. (2014). All new sequences were submitted to the EMBL nucleotide sequence database (accession numbers: LN555384- LN555522). The correspondence between MOTUs and the closest virtual taxa (VT) after BLAST search against the MaarjAM database (Öpik et al., 2010) is shown (JPEG 867 kb)

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Supplementary Fig. S9

Community diversity of arbuscular mycorrhizal fungi (AMF) shown as relative abundances of the 17 molecular operational taxonomic units (MOTUs) retrieved in (a) the soil and (b) the roots from three levels of intensification of land use: high intensity (HI; maize monoculture), low intensity (LI; extensive grassland) and zero intensity (ZI; agricultural soil left abandoned). AMF relative abundances from HI and ZI land-use types are from Pellegrino et al. (2014) (JPEG 423 kb)

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Ciccolini, V., Bonari, E. & Pellegrino, E. Land-use intensity and soil properties shape the composition of fungal communities in Mediterranean peaty soils drained for agricultural purposes. Biol Fertil Soils 51, 719–731 (2015). https://doi.org/10.1007/s00374-015-1013-4

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