Abstract
Arbuscular mycorrhizal (AM) fungal communities vary across habitat types, as well as across different land use types. Most relevant research, however, has focused on agricultural or other severely human-impacted ecosystems. Here, we compared AM fungal communities across six habitat types: calcareous grassland, overgrown ungrazed calcareous grassland, wooded meadow, farmyard lawn, boreonemoral forest, and boreonemoral forest clear-cut, exhibiting contrasting modes of land use. AM fungi in the roots of a single host plant species, Prunella vulgaris, and in its rhizosphere soil were identified using 454-sequencing from a total of 103 samples from 12 sites in Estonia. Mean AM fungal taxon richness per sample did not differ among habitats. AM fungal community composition, however, was significantly different among habitat types. Both abandonment and land use intensification (clearcutting; trampling combined with frequent mowing) changed AM fungal community composition. The AM fungal communities in different habitat types were most similar in the roots of the single host plant species and most distinct in soil samples, suggesting a non-random pattern in host-fungal taxon interactions. The results show that AM fungal taxon composition is driven by habitat type and land use intensity, while the plant host may act as an additional filter between the available and realized AM fungal species pool.
Similar content being viewed by others
References
Barwell LJ, Isaac NJB, Kunin WE (2015) Measuring β-diversity with species abundance data. J Anim Ecol 84(4):1112–1122. https://doi.org/10.1111/1365-2656.12362
Borriello R, Lumini E, Girlanda M et al (2012) Effects of different management practices on arbuscular mycorrhizal fungal diversity in maize fields by a molecular approach. Biol Fertil Soils 48(8):911–922. https://doi.org/10.1007/s00374-012-0683-4
Camacho C, Coulouris G, Avagyan V et al (2009) BLAST+: architecture and applications. BMC Bioinform 10(1):421. https://doi.org/10.1186/1471-2105-10-421
Camenzind T, Hempel S, Homeier J et al (2014) Nitrogen and phosphorus additions impact arbuscular mycorrhizal abundance and molecular diversity in a tropical montane forest. Glob Chang Biol 20(12):3646–3659. https://doi.org/10.1111/gcb.12618
Chagnon P-L, Bradley RL, Maherali H, Klironomos JN (2013) A trait-based framework to understand life history of mycorrhizal fungi. Trends Plant Sci 18(9):484–491. https://doi.org/10.1016/j.tplants.2013.05.001
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84(1):45–67. https://doi.org/10.1890/13-0133.1
Dai M, Bainard LD, Hamel C, Gan Y, Lynch D (2013) Impact of land use on arbuscular mycorrhizal fungal communities in rural Canada. Appl Environ Microbiol 79(21):6719–6729. https://doi.org/10.1128/AEM.01333-13
Davison J, Moora M, Öpik M et al (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349(6251):970–973. https://doi.org/10.1126/science.aab1161
Davison J, Moora M, Jairus T et al (2016) Hierarchical assembly rules in arbuscular mycorrhizal (AM) fungal communities. Soil Biol Biochem 97:63–70. https://doi.org/10.1016/j.soilbio.2016.03.003
Dumbrell AJ, Nelson M, Helgason T et al (2010) Relative roles of niche and neutral processes in structuring a soil microbial community. ISME J 4(3):337–345. https://doi.org/10.1038/ismej.2009.122
Edgar RC, Haas BJ, Clemente JC, Quince C, Knight R (2011) UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27(16):2194–2200. https://doi.org/10.1093/bioinformatics/btr381
García de León D, Moora M, Öpik M et al (2016) Symbiont dynamics during ecosystem succession: co-occurring plant and arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 92:fiw097. https://doi.org/10.1093/femsec/fiw097
Gazol A, Zobel M, Cantero JJ et al (2016) Impact of alien pines on local arbuscular mycorrhizal fungal communities—evidence from two continents. FEMS Microbiol Ecol 92:fiw073. https://doi.org/10.1093/femsec/fiw073
Grilli G, Urcelay C, Galetto L et al (2015) The composition of arbuscular mycorrhizal fungal communities in the roots of a ruderal forb is not related to the forest fragmentation process. Environ Microbiol 17(8):2709–2720. https://doi.org/10.1111/1462-2920.12623
Hamady M, Lozupone C, Knight R (2009) Fast UniFrac: facilitating high-throughput phylogenetic analyses of microbial communities including analysis of pyrosequencing and PhyloChip data. ISME J 4(1):17–27. https://doi.org/10.1038/ismej.2009.97
Hart MM, Reader RJ (2002) Taxonomic basis for variation in the colonization strategy of arbuscular mycorrhizal fungi. New Phytol 153(2):335–344. https://doi.org/10.1046/j.0028-646X.2001.00312.x
Helgason T, Daniell TJ, Husband R, Fitter AH, Young JPW (1998) Ploughing up the wood-wide web? Nature 394(6692):431. https://doi.org/10.1038/28764
Hempel S, Renker C, Buscot F (2007) Differences in the species composition of arbuscular mycorrhizal fungi in spore, root and soil communities in a grassland ecosystem. Environ Microbiol 9(8):1930–1938. https://doi.org/10.1111/j.1462-2920.2007.01309.x
Hodge A, Storer K (2015) Arbuscular mycorrhiza and nitrogen: implications for individual plants through to ecosystems. Plant Soil 386(1-2):1–19. https://doi.org/10.1007/s11104-014-2162-1
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7(12):1451–1456. https://doi.org/10.1111/2041-210X.12613
Jackson RB, Mooney HA, Schulze E-D (1997) A global budget for fine root biomass, surface area, and nutrient contents. Proc Natl Acad Sci 94(14):7362–7366. https://doi.org/10.1073/pnas.94.14.7362
Jansa J, Mozafar A, Kuhn G et al (2003) Soil tillage affects the community structure of mycorrhizal fungi in maize roots. Ecol Appl 13(4):1164–1176. https://doi.org/10.1890/1051-0761(2003)13[1164:STATCS]2.0.CO;2
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177(3):779–789. https://doi.org/10.1111/j.1469-8137.2007.02294.x
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(3):614–628. https://doi.org/10.1111/j.1469-8137.2012.04087.x
Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-induced resistance and priming of plant defenses. J Chem Ecol 38(6):651–664. https://doi.org/10.1007/s10886-012-0134-6
Kivlin SN, Hawkes CV, Treseder KK (2011) Global diversity and distribution of arbuscular mycorrhizal fungi. Soil Biol Biochem 43(11):2294–2303. https://doi.org/10.1016/j.soilbio.2011.07.012
Klironomos J, Zobel M, Tibbett M et al (2011) Forces that structure plant communities: quantifying the importance of the mycorrhizal symbiosis. New Phytol 189(2):366–370. https://doi.org/10.1111/j.1469-8137.2010.03550.x
Koorem K, Tulva I, Davison J et al (2017) Arbuscular mycorrhizal fungal communities in forest plant roots are simultaneously shaped by host characteristics and canopy-mediated light availability. Plant Soil 410(1-2):259–271. https://doi.org/10.1007/s11104-016-3004-0
Lee J, Lee S, Young JPW (2008) Improved PCR primers for the detection and identification of arbuscular mycorrhizal fungi. FEMS Microbiol Ecol 65(2):339–349. https://doi.org/10.1111/j.1574-6941.2008.00531.x
Liu Y, Mao L, Li J et al (2015) Resource availability differentially drives community assemblages of plants and their root-associated arbuscular mycorrhizal fungi. Plant Soil 386(1-2):341–355. https://doi.org/10.1007/s11104-014-2261-z
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71(12):8228–8235. https://doi.org/10.1128/AEM.71.12.8228-8235.2005
Lumini E, Orgiazzi A, Borriello R et al (2010) Disclosing arbuscular mycorrhizal fungal biodiversity in soil through a land-use gradient using a pyrosequencing approach. Environ Microbiol 12:2165–2179. https://doi.org/10.1111/j.1462-2920.2009.02099.x
McMurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS One 8(4):e61217. https://doi.org/10.1371/journal.pone.0061217
Mirás-Avalos JM, Antunes PM, Koch A, Khosla K, Klironomos JN, Dunfield KE (2011) The influence of tillage on the structure of rhizosphere and root-associated arbuscular mycorrhizal fungal communities. Pedobiologia 54(4):235–241. https://doi.org/10.1016/j.pedobi.2011.03.005
Moora M, Zobel M (2010) Arbuscular mycorrhizae and plant-plant interactions. In: Pugnaire FI (ed) Positive plant interactions and community dynamics. CRC Press, London, pp 79–98. https://doi.org/10.1093/aob/mcs269
Moora M, Davison J, Öpik M et al (2014) Anthropogenic land use shapes the composition and phylogenetic structure of soil arbuscular mycorrhizal fungal communities. FEMS Microbiol Ecol 90(3):609–621. https://doi.org/10.1111/1574-6941.12420
Morris EK, Buscot F, Herbst C et al (2013) Land use and host neighbor identity effects on arbuscular mycorrhizal fungal community composition in focal plant rhizosphere. Biodivers Conserv 22(10):2193–2205. https://doi.org/10.1007/s10531-013-0527-z
Neuenkamp L, Lewis RJ, Koorem K, Zobel K, Zobel M (2016) Changes in dispersal and light capturing traits explain post-abandonment community change in semi-natural grasslands. J Veg Sci 27(6):1222–1232. https://doi.org/10.1111/jvs.12449
Newbold T, Hudson LN, Hill SLL, Contu S, Lysenko I, Senior RA, Börger L, Bennett DJ, Choimes A, Collen B, Day J, de Palma A, Díaz S, Echeverria-Londoño S, Edgar MJ, Feldman A, Garon M, Harrison MLK, Alhusseini T, Ingram DJ, Itescu Y, Kattge J, Kemp V, Kirkpatrick L, Kleyer M, Correia DLP, Martin CD, Meiri S, Novosolov M, Pan Y, Phillips HRP, Purves DW, Robinson A, Simpson J, Tuck SL, Weiher E, White HJ, Ewers RM, Mace GM, Scharlemann JPW, Purvis A (2015) Global effects of land use on local terrestrial biodiversity. Nature 520(7545):45–50. https://doi.org/10.1038/nature14324
Newbold T, Hudson LN, Hill SLL, Contu S, Gray CL, Scharlemann JPW, Börger L, Phillips HRP, Sheil D, Lysenko I, Purvis A (2016) Global patterns of terrestrial assemblage turnover within and among land uses. Ecography 39(12):1151–1163. https://doi.org/10.1111/ecog.01932
Oksanen J, Blanchet F. G, Kindt R, et al (2015) Vegan: community ecology package. R package version 2.3–2. https://cran.r-project.org/package=vegan
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(4):778–790. https://doi.org/10.1111/j.1365-2745.2006.01136.x
Öpik M, Moora M, Zobel M et al (2008) High diversity of arbuscular mycorrhizal fungi in a boreal herb-rich coniferous forest. New Phytol 179(3):867–876. https://doi.org/10.1111/j.1469-8137.2008.02515.x
Öpik M, Metsis M, Daniell TJ et al (2009) Large-scale parallel 454 sequencing reveals host ecological group specificity of arbuscular mycorrhizal fungi in a boreonemoral forest. New Phytol 184(2):424–437. https://doi.org/10.1111/j.1469-8137.2009.02920.x
Öpik M, Vanatoa A, Vanatoa E et al (2010) The online database MaarjAM reveals global and ecosystemic distribution patterns in arbuscular mycorrhizal fungi (Glomeromycota). New Phytol 188(1):223–241. https://doi.org/10.1111/j.1469-8137.2010.03334.x
Öpik M, Davison J, Moora M, Zobel M (2014) DNA-based detection and identification of Glomeromycota: the virtual taxonomy of environmental sequences. Botany 92(2):135–147. https://doi.org/10.1139/cjb-2013-0110
Pärtel M, Wilson SD (2002) Root dynamics and spacial pattern in prairie and forest. Ecology 83(5):1199–1203. https://doi.org/10.1890/0012-9658(2002)083[1199:RDASPI]2.0.CO;2
Pinheiro J, Bates D, DebRoy S, et al (2017) {nlme}: linear and nonlinear mixed effects models. https://cran.r-project.org/package=nlme
Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205(4):1431–1436. https://doi.org/10.1111/nph.13252
R Core Team (2017) R: a language and environment for statistical computing. https://www.r-project.org/
Rillig MC, Aguilar-Trigueros CA, Bergmann J, Verbruggen E, Veresoglou SD, Lehmann A (2015) Plant root and mycorrhizal fungal traits for understanding soil aggregation. New Phytol 205(4):1385–1388. https://doi.org/10.1111/nph.13045
Rodriguez-Echeverria S, Teixeira H, Correia M et al (2017) Arbuscular mycorrhizal fungi communities from tropical Africa reveal strong ecological structure. New Phytol 213(1):380–390. https://doi.org/10.1111/nph.14122
Saks Ü, Davison J, Öpik M et al (2014) Root-colonizing and soil-borne communities of arbuscular mycorrhizal fungi in a temperate forest understorey. Botany 92(4):277–285. https://doi.org/10.1139/cjb-2013-0058
Säle V, Aguilera P, Laczko E et al (2015) Impact of conservation tillage and organic farming on the diversity of arbuscular mycorrhizal fungi. Soil Biol Biochem 84:38–52. https://doi.org/10.1016/j.soilbio.2015.02.005
Simon L, Lalonde M, Bruns TD (1992) Specific amplification of 18S fungal ribosomal genes from vesicular-arbuscular endomycorrhizal fungi colonizing roots. Appl Environ Microbiol 58:291–295
Simons NK, Lewinsohn T, Blüthgen N et al (2017) Contrasting effects of grassland management modes on species-abundance distributions of multiple groups. Agric Ecosyst Environ 237:143–153. https://doi.org/10.1016/j.agee.2016.12.022
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, Oxford
Smith SE, Anderson IC, Smith FA (2015) Mycorrhizal associations and phosphorus acquisition: from cells to ecosystems. In: Plaxton WC, Lambers H (eds) Annual plant reviews, vol 48. John Wiley & Sons, Inc, Hoboken, pp 409–439. https://doi.org/10.1002/9781118958841.ch14
Spatafora JW, Chang Y, Benny GL et al (2016) A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia 108(5):1028–1046. https://doi.org/10.3852/16-042
Treseder KK (2016) Model behavior of arbuscular mycorrhizal fungi: predicting soil carbon dynamics under climate change. Botany 94(6):417–423. https://doi.org/10.1139/cjb-2015-0245
Uibopuu A, Moora M, Öpik M, Zobel M (2012) Temperate forest understorey species performance is altered by local arbuscular mycorrhizal fungal communities from stands of different successional stages. Plant Soil 356(1-2):331–339. https://doi.org/10.1007/s11104-011-1116-0
Vályi K, Rillig MC, Hempel S (2015) Land-use intensity and host plant identity interactively shape communities of arbuscular mycorrhizal fungi in roots of grassland plants. New Phytol 205(4):1577–1586. https://doi.org/10.1111/nph.13236
Varela-Cervero S, Vasar M, Davison J et al (2015) The composition of arbuscular mycorrhizal fungal communities differs among the roots, spores and extraradical mycelia associated with five Mediterranean plant species. Environ Microbiol 17(8):2882–2895. https://doi.org/10.1111/1462-2920.12810
Verbruggen E, Van Der Heijden MGA, Weedon JT et al (2012) Community assembly, species richness and nestedness of arbuscular mycorrhizal fungi in agricultural soils. Mol Ecol 21(10):2341–2353. https://doi.org/10.1111/j.1365-294X.2012.05534.x
Werner GDA, Kiers ET (2015) Partner selection in the mycorrhizal mutualism. New Phytol 205(4):1437–1442. https://doi.org/10.1111/nph.13113
Xiang D, Verbruggen E, Hu Y, Veresoglou SD, Rillig MC, Zhou W, Xu T, Li H, Hao Z, Chen Y, Chen B (2014) Land use influences arbuscular mycorrhizal fungal communities in the farming—pastoral ecotone of northern China. New Phytol 204(4):968–978. https://doi.org/10.1111/nph.12961
Zobel M, Öpik M (2014) Plant and arbuscular mycorrhizal fungal (AMF) communities–which drives which? J Veg Sci 25(5):1133–1140. https://doi.org/10.1111/jvs.12191
Acknowledgements
We are grateful to John Davison, Guillermo Bueno, and David García de León for the advice on statistical analyses, Robert Szava-Kovats for the linguistic advice, Ülle Saks for the help in the laboratory, and Anu Lepik for the support with fieldwork. We thank the editor and two anonymous referees for comments on the manuscript. This study was funded by the Estonian Research Council (IUT 20-28) and by the European Regional Development Fund (Centre of Excellence EcolChange).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Electronic supplementary material
ESM 1
(PDF 3129 kb)
Rights and permissions
About this article
Cite this article
Sepp, SK., Jairus, T., Vasar, M. et al. Effects of land use on arbuscular mycorrhizal fungal communities in Estonia. Mycorrhiza 28, 259–268 (2018). https://doi.org/10.1007/s00572-018-0822-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-018-0822-3