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Range-expansion effects on the belowground plant microbiome

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

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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.

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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.

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.

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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.).

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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

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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.

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Correspondence to Kelly S. Ramirez.

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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

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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

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