Letter | Published:

Leaf bacterial diversity mediates plant diversity and ecosystem function relationships

Nature volume 546, pages 145147 (01 June 2017) | Download Citation

Abstract

Research on biodiversity and ecosystem functioning has demonstrated links between plant diversity and ecosystem functions such as productivity1,2. At other trophic levels, the plant microbiome has been shown to influence host plant fitness and function3,4, and host-associated microbes have been proposed to influence ecosystem function through their role in defining the extended phenotype of host organisms5,6 However, the importance of the plant microbiome for ecosystem function has not been quantified in the context of the known importance of plant diversity and traits. Here, using a tree biodiversity–ecosystem functioning experiment, we provide strong support for the hypothesis that leaf bacterial diversity is positively linked to ecosystem productivity, even after accounting for the role of plant diversity. Our results also show that host species identity, functional identity and functional diversity are the main determinants of leaf bacterial community structure and diversity. Our study provides evidence of a positive correlation between plant-associated microbial diversity and terrestrial ecosystem productivity, and a new mechanism by which models of biodiversity–ecosystem functioning relationships can be improved.

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References

  1. 1.

    , & Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory. Proc. Natl Acad. Sci. USA 109, 10394–10397 (2012)

  2. 2.

    . et al. Positive biodiversity-productivity relationship predominant in global forests. Science 354, aaf8957 (2016)

  3. 3.

    , , , & The importance of the microbiome of the plant holobiont. New Phytol. 206, 1196–1206 (2015)

  4. 4.

    Microbial life in the phyllosphere. Nat. Rev. Microbiol. 10, 828–840 (2012)

  5. 5.

    & Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics. Front. Microbiol. 6, 486 (2015)

  6. 6.

    , , & The plant microbiota: systems biology insights and perspectives. Annu. Rev. Genet. 50, 211–234 (2016)

  7. 7.

    et al. Plant ecology. Anthropogenic environmental changes affect ecosystem stability via biodiversity. Science 348, 336–340 (2015)

  8. 8.

    et al. Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition. Ecol. Lett. 18, 834–843 (2015)

  9. 9.

    & Partitioning selection and complementarity in biodiversity experiments. Nature 412, 72–76 (2001)

  10. 10.

    , , , & Functional and phylogenetic diversity as predictors of biodiversity–ecosystem-function relationships. Ecology 92, 1573–1581 (2011)

  11. 11.

    et al. A general biodiversity–function relationship is mediated by trophic level. Oikos 126, 18–31 2016)

  12. 12.

    et al. Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice. ISME J. 6, 1378–1390 (2012)

  13. 13.

    et al. Bacterial communities in the phylloplane of Prunus species. J. Basic Microbiol. 55, 504–508 (2015)

  14. 14.

    et al. Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer. New Phytol. 210, 657–668 (2016)

  15. 15.

    , , & A synthetic community approach reveals plant genotypes affecting the phyllosphere microbiota. PLoS Genet. 10, e1004283 (2014)

  16. 16.

    & Modulation of host immunity by beneficial microbes. Mol. Plant Microbe Interact. 25, 139–150 (2012)

  17. 17.

    et al. A novel microbiome therapeutic increases gut microbial diversity and prevents recurrent Clostridium difficile infection. J. Infect. Dis. 214, 173–181 (2016)

  18. 18.

    , & The rhizosphere microbiome and plant health. Trends Plant Sci. 17, 478–486 (2012)

  19. 19.

    et al. Microbial hub taxa link host and abiotic factors to plant microbiome variation. PLoS Biol. 14, e1002352 (2016)

  20. 20.

    et al. The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. New Phytol. 210, 1033–1043 (2016)

  21. 21.

    , & Heterogeneous transcription of an indoleacetic acid biosynthetic gene in Erwinia herbicola on plant surfaces. Proc. Natl Acad. Sci. USA 98, 3454–3459 (2001)

  22. 22.

    & Contribution of indole-3-acetic acid production to the epiphytic fitness of Erwinia herbicola. Appl. Environ. Microbiol. 64, 3256–3263 (1998)

  23. 23.

    , & Host species identity, site and time drive temperate tree phyllosphere bacterial community structure. Microbiome 4, 27 (2016)

  24. 24.

    et al. Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest. Proc. Natl Acad. Sci. USA 111, 13715–13720 (2014)

  25. 25.

    , , , & Tropical tree diversity enhances light capture through crown plasticity and spatial and temporal niche differences. Ecology 95, 2479–2492 (2014)

  26. 26.

    et al. From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment. Proc. R. Soc. B 274, 871–876 (2007)

  27. 27.

    , & Trophic complementarity drives the biodiversity-ecosystem functioning relationship in food webs. Ecol. Lett. 16, 853–861 (2013)

  28. 28.

    , & Dispersal of Bacillus subtilis and its effect on strawberry phyllosphere microbiota under open field and protection conditions. Sci. Rep. 6, 22611 (2016)

  29. 29.

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

  30. 30.

    , , , & Advancing biodiversity-ecosystem functioning science using high-density tree-based experiments over functional diversity gradients. Oecologia 174, 609–621 (2014)

  31. 31.

    et al. Contributions of a global network of tree diversity experiments to sustainable forest plantations. Ambio 45, 29–41 (2016)

  32. 32.

    et al. Functional identity is the main driver of diversity effects in young tree communities. Ecol. Lett. 19, 638–647 (2016)

  33. 33.

    & A distance-based framework for measuring functional diversity from multiple traits. Ecology 91, 299–305 (2010)

  34. 34.

    et al. Assessing functional diversity in the field–methodology matters! Funct. Ecol. 22, 134–147 (2008)

  35. 35.

    et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6 (2014)

  36. 36.

    , , , & The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. Environ. Microbiol. 12, 2885–2893 (2010)

  37. 37.

    , , & PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30, 614–620 (2014)

  38. 38.

    et al. QIIME allows analysis of high-throughput community sequencing data. Nat. Met. 7, 335–336 (2010)

  39. 39.

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

  40. 40.

    et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069–5072 (2006)

  41. 41.

    ., . & APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290 (2004)

  42. 42.

    et al. Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26, 1463–1464 (2010)

  43. 43.

    et al. The vegan package. Community Ecology Package 10, 631–637 (2007)

  44. 44.

    R Development Core Team. R: A Language and Environment for Statistical Computing; (Vienna, Austria, 2013)

  45. 45.

    & A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol. Evol. 4, 133–142 (2013)

  46. 46.

    Extension of Nakagawa & Schielzeth’s R(2)GLMM to random slopes models. Methods Ecol. Evol. 5, 944–946 (2014)

  47. 47.

    et al. Towards a worldwide wood economics spectrum. Ecol. Lett. 12, 351–366 (2009)

  48. 48.

    & Tolerance to shade, drought and waterlogging of temperate, northern hemisphere trees and shrubs. Ecol. Monogr. 76, 521–547 (2006)

  49. 49.

    Royal Botanic Gardens Kew. Seed Information Database (SID) version 7.1; (2008)

  50. 50.

    et al. The worldwide leaf economics spectrum. Nature 428, 821–827 (2004)

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Acknowledgements

We are grateful to R. Fréchon, S. Guérard and M. A. Chadid Hernandez for their help in the field, and to J. Shapiro and his laboratory for technical support. We also thank B. Shipley for his help with structural equation modelling techniques used in the manuscript. C. M. Tobner, P. B. Reich and D. Gravel helped in designing the original experiment (IDENT-Montréal) together with A.P. and C.M. The study site is part of McGill University and we much appreciate their support.

Author information

Affiliations

  1. Département des Sciences Biologiques, Université du Québec à Montréal, Montréal H3C 3P8, Québec, Canada

    • Isabelle Laforest-Lapointe
    • , Alain Paquette
    • , Christian Messier
    •  & Steven W. Kembel
  2. Centre d’étude de la Forêt, Université du Québec à Montréal, Montréal H2X 3Y7, Québec, Canada

    • Isabelle Laforest-Lapointe
    • , Alain Paquette
    • , Christian Messier
    •  & Steven W. Kembel
  3. Institut des Sciences de la Forêt Tempérée, Université du Québec en Outaouais, Ripon J0V 1V0, Québec, Canada

    • Christian Messier

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Contributions

I.L.-L., C.M. and S.W.K. designed the study; C.M. and A.P. established the field experiment; I.L.-L. collected the data; I.L.-L. analysed the data with support from A.P. and S.W.K.; all authors contributed to the writing of the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Isabelle Laforest-Lapointe.

Reviewer Information Nature thanks D. Wardle, S. Lindow, J. Grace and the other anonymous reviewer(s) for their contribution to the peer review of this work.

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https://doi.org/10.1038/nature22399

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