Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Range-expansion effects on the belowground plant microbiome

Nature Ecology & Evolution volume 3, pages 604–611 (2019)Cite this article

Subjects

Abstract

Plant range expansion is occurring at a rapid pace, largely in response to human-induced climate warming. Although the movement of plants along latitudinal and altitudinal gradients is well-documented, effects on belowground microbial communities remain largely unknown. Furthermore, for range expansion, not all plant species are equal: in a new range, the relatedness between range-expanding plant species and native flora can influence plant–microorganism interactions. Here we use a latitudinal gradient spanning 3,000 km across Europe to examine bacterial and fungal communities in the rhizosphere and surrounding soils of range-expanding plant species. We selected range-expanding plants with and without congeneric native species in the new range and, as a control, the congeneric native species, totalling 382 plant individuals collected across Europe. In general, the status of a plant as a range-expanding plant was a weak predictor of the composition of bacterial and fungal communities. However, microbial communities of range-expanding plant species became more similar to each other further from their original range. Range-expanding plants that were unrelated to the native community also experienced a decrease in the ratio of plant pathogens to symbionts, giving weak support to the enemy release hypothesis. Even at a continental scale, the effects of plant range expansion on the belowground microbiome are detectable, although changes to specific taxa remain difficult to decipher.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Changes in microbial community during plant range expansions.
Fig. 2: The rhizosphere and soil contain different microbial communities.
Fig. 3: Plant species was the strongest predictor of bacterial and fungal community structure in both the soil and the rhizosphere.
Fig. 4: Changes in microbial community dissimilarly across the range-expansion gradient.
Fig. 5: Changes in alpha diversity across the latitudinal gradient of range expansion differs between bacterial and fungal communities.

Similar content being viewed by others

Data availability

The authors declare that the data supporting the findings of this study are available within the paper and its Supplementary Information. Sequences have been deposited in the European Nucleotide Archive under accession numbers PRJEB25697, PRJEB25694, PRJEB25693 and PRJEB25692.

References

  1. Pecl, G. T. et al. Biodiversity redistribution under climate change: impacts on ecosystems and human well-being. Science 355, eaai9214 (2017).

  2. Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).

    Article  CAS  Google Scholar 

  3. Classen, A. T. et al. Direct and indirect effects of climate change on soil microbial and soil microbial–plant interactions: what lies ahead? Ecosphere 6, art130 (2015).

    Article  Google Scholar 

  4. Meisner, A., De Deyn, G. B., de Boer, W. & van der Putten, W. H. Soil biotic legacy effects of extreme weather events influence plant invasiveness. Proc. Natl Acad. Sci. USA 110, 9835–9838 (2013).

    Article  CAS  Google Scholar 

  5. Engelkes, T. et al. Successful range-expanding plants experience less above-ground and below-ground enemy impact. Nature 456, 946–948 (2008).

    Article  CAS  Google Scholar 

  6. van der Putten, W. H., Bradford, M. A., Brinkman, E. P., van de Voorde, T. F. J. & Veen, G. F. Where, when and how plant–soil feedback matters in a changing world. Funct. Ecol. 30, 1109–1121 (2016).

    Article  Google Scholar 

  7. Gonzalez-Megias, A. & Menendez, R. Climate change effects on above- and below-ground interactions in a dryland ecosystem. Phil. Trans. R. Soc. B 367, 3115–3124 (2012).

    Article  Google Scholar 

  8. Tylianakis, J. M., Didham, R. K., Bascompte, J. & Wardle, D. A. Global change and species interactions in terrestrial ecosystems. Ecol. Lett. 11, 1351–1363 (2008).

    Article  Google Scholar 

  9. Kourtev, P. S., Ehrenfeld, J. G. & Häggblom, M. Exotic plant species alter the microbial community structure and function in the soil. Ecology 83, 3152–3166 (2002).

    Article  Google Scholar 

  10. McLeod, M. L. et al. Exotic invasive plants increase productivity, abundance of ammonia-oxidizing bacteria and nitrogen availability in intermountain grasslands. J. Ecol. 104, 994–1002 (2016).

    Article  CAS  Google Scholar 

  11. Coats, V. C. & Rumpho, M. E. The rhizosphere microbiota of plant invaders: an overview of recent advances in the microbiomics of invasive plants. Front. Microbiol. 5, 368 (2014).

    Article  Google Scholar 

  12. Klironomos, J. N. Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417, 67–70 (2002).

    Article  CAS  Google Scholar 

  13. Kardol, P. & Wardle, D. A. How understanding aboveground–belowground linkages can assist restoration ecology. Trends Ecol. Evol. 25, 670–679 (2010).

    Article  Google Scholar 

  14. Van Nuland, M. E., Bailey, J. K. & Schweitzer, J. A. Divergent plant–soil feedbacks could alter future elevation ranges and ecosystem dynamics. Nat. Ecol. Evol. 1, 0150 (2017).

    Article  Google Scholar 

  15. van Grunsven, R. H. A. et al. Reduced plant–soil feedback of plant species expanding their range as compared to natives. J. Ecol. 95, 1050–1057 (2007).

    Article  Google Scholar 

  16. Dostálek, T., Münzbergová, Z., Kladivová, A. & Macel, M. Plant–soil feedback in native vs. invasive populations of a range expanding plant. Plant Soil 399, 209–220 (2015).

  17. Berg, G. & Smalla, K. Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere. FEMS Microbiol. Ecol. 68, 1–13 (2009).

    Article  CAS  Google Scholar 

  18. De Frenne, P. et al. Plant movements and climate warming: intraspecific variation in growth responses to nonlocal soils. New Phytol. 202, 431–441 (2014).

    Article  Google Scholar 

  19. Van Grunsven, R. H. A., van der Putten, W. H., Bezemer, T., Berendse, F. & Veenendaal, E. M. Plant–soil interactions in the expansion and native range of a poleward shifting plant species. Glob. Change Biol. 16, 380–385 (2010).

    Article  Google Scholar 

  20. Collins, C. G., Carey, C. J., Aronson, E. L., Kopp, C. W. & Diez, J. M. Direct and indirect effects of native range expansion on soil microbial community structure and function. J. Ecol. 104, 1271–1283 (2016).

    Article  Google Scholar 

  21. Fierer, N. Embracing the unknown: disentangling the complexities of the soil microbiome. Nat. Rev. Microbiol. 15, 579–590 (2017).

    Article  CAS  Google Scholar 

  22. Kuramae, E., Gamper, H., van Veen, J. & Kowalchuk, G. Soil and plant factors driving the community of soil-borne microorganisms across chronosequences of secondary succession of chalk grasslands with a neutral pH. FEMS Microbiol. Ecol. 77, 285–294 (2011).

    Article  CAS  Google Scholar 

  23. Tecon, R. & Or, D. Biophysical processes supporting the diversity of microbial life in soil. FEMS Microbiol. Rev. 41, 599–623 (2017).

    Article  CAS  Google Scholar 

  24. Lauber, C. L., Hamady, M., Knight, R. & Fierer, N. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl. Environ. Microbiol. 75, 5111–5120 (2009).

    Article  CAS  Google Scholar 

  25. Delgado-Baquerizo, M. et al. A global atlas of the dominant bacteria found in soil. Science 359, 320–325 (2018).

    Article  CAS  Google Scholar 

  26. Talbot, J. M. et al. Endemism and functional convergence across the North American soil mycobiome. Proc. Natl Acad. Sci. USA 111, 6341–6346 (2014).

    Article  CAS  Google Scholar 

  27. Tedersoo, L. et al. Global diversity and geography of soil fungi. Science 346, 1256688 (2014).

  28. Barberán, A. et al. Why are some microbes more ubiquitous than others? Predicting the habitat breadth of soil bacteria. Ecol. Lett. 17, 794–802 (2014).

  29. Lekberg, Y., Rosendahl, S. & Olsson, P. A. The fungal perspective of arbuscular mycorrhizal colonization in ‘nonmycorrhizal’ plants. New Phytol. 205, 1399–1403 (2015).

    Article  Google Scholar 

  30. Lau, J. A. & Lennon, J. T. Rapid responses of soil microorganisms improve plant fitness in novel environments. Proc. Natl Acad. Sci. USA 109, 14058–14062 (2012).

    Article  CAS  Google Scholar 

  31. de Vries, F. T. et al. Land use alters the resistance and resilience of soil food webs to drought. Nat. Clim. Change 2, 276–280 2012).

    Article  Google Scholar 

  32. Peay, K. G. Back to the future: natural history and the way forward in modern fungal ecology. Fungal Ecol. 12, 4–9 (2014).

    Article  Google Scholar 

  33. Edwards, J. et al. Structure, variation, and assembly of the root-associated microbiomes of rice. Proc. Natl Acad. Sci. USA 112, E911–E920 (2015).

    Article  CAS  Google Scholar 

  34. Pieterse, C. M. J., de Jonge, R. & Berendsen, R. L. The soil-borne supremacy. Trends Plant Sci. 21, 171–173 (2016).

    Article  CAS  Google Scholar 

  35. Prober, S. M. et al. Plant diversity predicts beta but not alpha diversity of soil microbes across grasslands worldwide. Ecol. Lett. 18, 85–95 (2015).

    Article  Google Scholar 

  36. Gilbert, G. S. & Webb, C. O. Phylogenetic signal in plant pathogen–host range. Proc. Natl Acad. Sci. USA 104, 4979–4983 (2007).

    Article  CAS  Google Scholar 

  37. Parker, I. M. et al. Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520, 542–544 (2015).

    Article  CAS  Google Scholar 

  38. Lankau, R. A. Coevolution between invasive and native plants driven by chemical competition and soil biota. Proc. Natl Acad. Sci. USA 109, 11240–11245 (2012).

    Article  CAS  Google Scholar 

  39. Morriën, E. et al. Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun. 8, 14349 (2017).

    Article  Google Scholar 

  40. Keymer, D. P. & Lankau, R. A. Disruption of plant–soil–microbial relationships influences plant growth. J. Ecol. 105, 816–827 (2017).

    Article  CAS  Google Scholar 

  41. Leach, J. E., Triplett, L. R., Argueso, C. T. & Trivedi, P. Communication in the phytobiome. Cell 169, 587–596 (2017).

    Article  CAS  Google Scholar 

  42. Bakkenes, M., Alkemade, J. R. M., Ihle, F., Leemans, R. & Latour, J. B. Assessing effects of forecasted climate change on the diversity and distribution of European higher plants for 2050. Glob. Change Biol. 8, 390–407 (2002).

    Article  Google Scholar 

  43. Wilschut, R. A., Kostenko, O., Koorem, K. & van der Putten, W. H. Nematode community responses to range-expanding and native plant communities in original and new range soils. Ecol. Evol. 8, 10288–10297 (2018).

  44. Koorem, K. et al. Relatedness with plant species in native community influences ecological consequences of range expansions. Oikos 127, 981–990 (2018).

  45. van der Heijden, M. G. A. & Hartmann, M. Networking in the plant microbiome. PLoS Biol. 14, e1002378 (2016).

  46. Leff, J. W. et al. Predicting the structure of soil communities from plant community taxonomy, phylogeny, and traits. ISME J. 12, 1794–1805 (2018).

  47. Fierer, N. et al. Reconstructing the Microbial diversity and function of pre-agricultural tallgrass prairie soils in the United States. Science 342, 621–624 (2013).

    Article  CAS  Google Scholar 

  48. Emmett, B. D., Youngblut, N. D., Buckley, D. H. & Drinkwater, L. E. Plant phylogeny and life history shape rhizosphere bacterial microbiome of summer annuals in an agricultural field. Front. Microbiol. 8, 2414 (2017).

    Article  Google Scholar 

  49. Goberna, M., Navarro-Cano, J. A. & Verdú, M. Opposing phylogenetic diversity gradients of plant and soil bacterial communities. Proc. R. Soc. B 283, 20153003 (2016).

    Article  Google Scholar 

  50. Reynolds, H. L., Packer, A., Bever, J. D. & Clay, K. Grassroots ecology: plant–microbe–soil interactions as drivers of plant community structure and dynamics. Ecology 84, 2281–2291 (2003).

    Article  Google Scholar 

  51. Bennett, J. A. et al. Plant–soil feedbacks and mycorrhizal type influence temperate forest population dynamics. Science 355, 181–184 (2017).

  52. Golivets, M. & Wallin, K. F. Neighbour tolerance, not suppression, provides competitive advantage to non-native plants. Ecol. Lett. 21, 745–759 (2018).

  53. Geml, J. & Wagner, M. R. Out of sight, but no longer out of mind — towards an increased recognition of the role of soil microbes in plant speciation. New Phytol. 217, 965–967 (2018).

    Article  Google Scholar 

  54. Dawson, W. Release from belowground enemies and shifts in root traits as interrelated drivers of alien plant invasion success: a hypothesis. Ecol. Evol. 5, 4505–4516 (2015).

    Article  Google Scholar 

  55. Blumenthal, D., Mitchell, C. E., Pysek, P. & Jarosík, V. Synergy between pathogen release and resource availability in plant invasion. Proc. Natl Acad. Sci. USA 106, 7899–7904 (2009).

    Article  CAS  Google Scholar 

  56. Wilschut, R. A., Silva, J. C. P., Garbeva, P. & van der Putten, W. H. Belowground plant–herbivore interactions vary among climate-driven range-expanding plant species with different degrees of novel chemistry. Front. Plant Sci. 8, 1861 (2017).

    Article  Google Scholar 

  57. Inderjit & van der Putten, W. H. Impacts of soil microbial communities on exotic plant invasions. Trends Ecol. Evol. 25, 512–519 (2010).

    Article  CAS  Google Scholar 

  58. Rout, M. E. & Callaway, R. M. Interactions between exotic invasive plants and soil microbes in the rhizosphere suggest that ‘everything is not everywhere’. Ann. Bot 110, 213–222 (2012).

    Article  Google Scholar 

  59. Nguyen, N. H. et al. FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol. 20, 241–248 (2016).

    Article  Google Scholar 

  60. van der Putten, W. H. Climate change, aboveground–belowground interactions, and species’ range shifts. Annu. Rev. Ecol. Evol. Syst. 43, 365–383 (2012).

  61. Mitchell, C. E. & Power, A. G. Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627 (2003).

    Article  CAS  Google Scholar 

  62. Bever, J. D., Mangan, S. A. & Alexander, H. M. Maintenance of plant species diversity by pathogens. Annu. Rev. Ecol. Evol. Syst. 46, 305–325 (2015).

    Article  Google Scholar 

  63. Morriën, E. et al. Soil networks become more connected and take up more carbon as nature restoration progresses. Nat. Commun. 8, 14349 (2017).

    Article  Google Scholar 

  64. Hannula, S. E. et al. Shifts in rhizosphere fungal community during secondary succession following abandonment from agriculture. ISME J. 11, 2294–2304 (2017).

    Article  Google Scholar 

  65. Jousset, A. et al. Where less may be more: how the rare biosphere pulls ecosystems strings. ISME J. 11, 853–862 (2017).

    Article  Google Scholar 

  66. van Kleunen, M., Dawson, W. & Maurel, N. Characteristics of successful alien plants. Mol. Ecol. 24, 1954–1968 (2015).

    Article  Google Scholar 

  67. Chen, I.-C., Hill, J. K., Ohlemuller, R., Roy, D. B. & Thomas, C. D. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024–1026 (2011).

    Article  CAS  Google Scholar 

  68. Bever, J., Platt, T. & Morton, E. Microbial population and community dynamics on plant roots and their feedbacks on plant communities. Annu. Rev. Microbiol. 66, 265–283 (2012).

    Article  CAS  Google Scholar 

  69. Wubs, E. R. J., van der Putten, W. H., Bosch, M. & Bezemer, T. M. Soil inoculation steers restoration of terrestrial ecosystems. Nat. Plants 2, 16107 (2016).

    Article  Google Scholar 

  70. Alexander, J. M., Diez, J. M. & Levine, J. M. Novel competitors shape species’ responses to climate change. Nature 525, 515–518 (2015).

    Article  CAS  Google Scholar 

  71. Fordham, D. A. et al. Plant extinction risk under climate change: are forecast range shifts alone a good indicator of species vulnerability to global warming? Glob. Change Biol. 18, 1357–1371 (2012).

    Article  Google Scholar 

  72. Tamis, W. L. M., van’t Zelfde, M., van der Meijden, R. & de Haes, H. A. U. Changes in vascular plant biodiversity in the Netherlands in the 20th century explained by their climatic and other environmental characteristics. Climatic Change 72, 37–56 (2005).

    Article  Google Scholar 

  73. Caporaso, J. G. et al. Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J. 6, 1621–1624 (2012).

    Article  CAS  Google Scholar 

  74. Ihrmark, K. et al. New primers to amplify the fungal ITS2 region—evaluation by 454-sequencing of artificial and natural communities. FEMS Microbiol. Ecol. 82, 666–677 (2012).

    Article  CAS  Google Scholar 

  75. Lundberg, D. S., Yourstone, S., Mieczkowski, P., Jones, C. D. & Dangl, J. L. Practical innovations for high-throughput amplicon sequencing. Nat. Methods 10, 999–1002 (2013).

    Article  CAS  Google Scholar 

  76. Masella, A. P., Bartram, A. K., Truszkowski, J. M., Brown, D. G. & Neufeld, J. D. PANDAseq: paired-end assembler for illumina sequences. BMC Bioinformatics 13, 31 (2012).

    Article  CAS  Google Scholar 

  77. Dodt, M., Roehr, J., Ahmed, R. & Dieterich, C. FLEXBAR—flexible barcode and adapter processing for next-generation sequencing platforms. Biology (Basel) 1, 895–905 (2012).

    Google Scholar 

  78. Rognes, T., Flouri, T., Nichols, B., Quince, C. & Mahé, F. VSEARCH: a versatile open source tool for metagenomics. PeerJ 4, e2584 (2016).

    Article  Google Scholar 

  79. Edgar, R. C. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26, 2460–2461 (2010).

    Article  CAS  Google Scholar 

  80. Edgar, R. C., Haas, B. J., Clemente, J. C., Quince, C. & Knight, R. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 27, 2194–2200 (2011).

    Article  CAS  Google Scholar 

  81. Cole, J. R. et al. Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res. 42, D633–D642 (2014).

    Article  CAS  Google Scholar 

  82. Bengtsson-Palme, J. et al. Improved software detection and extraction of ITS1 and ITS2 from ribosomal ITS sequences of fungi and other eukaryotes for analysis of environmental sequencing data. Methods Ecol. Evol. 4, 914–919 (2013).

    Google Scholar 

  83. Kõljalg, U. et al. Towards a unified paradigm for sequence-based identification of fungi. Mol. Ecol. 22, 5271–5277 (2013).

    Article  Google Scholar 

  84. Koster, J. & Rahmann, S. Snakemake—a scalable bioinformatics workflow engine. Bioinformatics 28, 2520–2522 (2012).

    Article  Google Scholar 

  85. Oksanen, J. et al. vegan: Community Ecology Package. R package version 2.0-10 https://cran.r-project.org/web/packages/vegan/index.html (2013).

  86. Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).

Download references

Acknowledgements

We are grateful for the support of Ž. Modrić-Surina, S. Dragićević, I. Starke and M. Hohla, who all helped with sampling. This work was supported in large part by the European Research Council (ERC advanced grant ERC-Adv 323020 (SPECIALS) to W.H.v.d.P. Additional support came from the Estonian Research Council (grant PUTJD78) (K.K.) and the Slovenian Research Agency (research core funding no. P1-0236) (B.V. and T.Č.).

Author information

Authors and Affiliations

  1. Netherlands Institute of Ecology, Wageningen, the Netherlands

    Kelly S. Ramirez, L. Basten Snoek, Kadri Koorem, Stefan Geisen, L. Janneke Bloem, Freddy ten Hooven, Olga Kostenko, Marta Manrubia, Debbie van Raaij, Carolin Weser, Rutger A. Wilschut & Wim H. van der Putten

  2. Theoretical Biology and Bioinformatics, Utrecht University, Utrecht, the Netherlands

    L. Basten Snoek

  3. Laboratory of Nematology, Wageningen University, Wageningen, the Netherlands

    L. Basten Snoek, Rutger A. Wilschut & Wim H. van der Putten

  4. Department of Botany, Institute of Ecology and Earth Sciences, University of Tartu, Tartu, Estonia

    Kadri Koorem

  5. Department of Plant Sciences, Wageningen University & Research, Wageningen, the Netherlands

    L. Janneke Bloem

  6. Department of Ecology, School of Biology, Aristotle University, Thessaloniki, Greece

    Nikos Krigas & Maria A. Tsiafouli

  7. Institute of Plant Breeding and Genetic Resources, Hellenic Agricultural Organization Demeter, Thessaloniki, Greece

    Nikos Krigas

  8. Department of Biology, Faculty of Natural Sciences and Mathematics, University of Montenegro, Podgorica, Montenegro

    Danka Caković

  9. Biološki inštitut Jovana Hadžija, ZRC SAZU, Ljubljana, Slovenia

    Branko Vreš & Tatjana Čelik

Authors
  1. Kelly S. Ramirez
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. Basten Snoek
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Kadri Koorem
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Stefan Geisen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. L. Janneke Bloem
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Freddy ten Hooven
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Olga Kostenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Nikos Krigas
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Marta Manrubia
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Danka Caković
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Debbie van Raaij
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Maria A. Tsiafouli
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Branko Vreš
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Tatjana Čelik
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Carolin Weser
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Rutger A. Wilschut
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Wim H. van der Putten
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

W.H.v.d.P. conceived the idea of this study. Sample collection was completed W.H.v.d.P., K.S.R., K.K., S.G., L.J.B., F.t.H., O.K., N.K., M.M., D.C., M.A.T., B.V., T.Č., C.W. and R.A.W. Soil analyses and sequencing were completed by L.J.B., F.t.H., C.W., D.v.R. and K.S.R. Data analyses were completed by L.B.S. and K.S.R. The manuscript was written by K.S.R., with contributions from all co-authors.

Corresponding author

Correspondence to Kelly S. Ramirez.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Supplementary Information

Supplementary Tables 1–7 and Supplementary Figures 1–3

Reporting Summary

Supplementary Data 1

OTU tables: microbial taxa (OTUs) abundances

Supplementary Data 2

Environmental Factors by sample: all samples with plant information, soil abiotic factors and locations

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ramirez, K.S., Snoek, L.B., Koorem, K. et al. Range-expansion effects on the belowground plant microbiome. Nat Ecol Evol 3, 604–611 (2019). https://doi.org/10.1038/s41559-019-0828-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41559-019-0828-z

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing