Leaf bacterial diversity mediates plant diversity and ecosystem function relationships

Journal name:
Nature
Volume:
546,
Pages:
145–147
Date published:
DOI:
doi:10.1038/nature22399
Received
Accepted
Published online

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.

At a glance

Figures

  1. The IDENT experiment near Montreal, Canada.
    Figure 1: The IDENT experiment near Montreal, Canada.

    A total of 54 community mixtures involving 19 tree species replicated four times were established in spring 2009, including gradients of species richness (1, 2, 4 and 12) and functional diversity (8 initial levels). The functional diversity of all possible mixtures was ordered into 8 bins from which communities were chosen. Smaller white squares placed as exponents denote additional plots at some functional diversity levels (different communities producing similar functional diversity values). Exotic species were included as monocultures and in mixtures of 4 and 12 with native species in equal proportion, denoted as subscript black squares. IDENT, International Diversity Experiment Network with Trees.

  2. Structural equation model of plant diversity and identity explaining leaf bacterial diversity and plant community productivity.
    Figure 2: Structural equation model of plant diversity and identity explaining leaf bacterial diversity and plant community productivity.

    The path analysis (n = 216, χ2 = 1.451, P = 0.484, degrees of freedom (df) = 2; root mean square error of approximation (RMSEA) = 0.00, P = 0.644) explains 41% of the variance in leaf bacterial diversity and 85% of the variance in plot productivity. Numbers adjacent to arrows and arrow width indicate the relationship’s effect size and the associated bootstrap P value. +P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001. Black and grey arrows indicate positive and negative relationships, respectively.

  3. Identity of the tree host species in each of the 54 combinations at the IDENT experiment in Montreal.
    Extended Data Fig. 1: Identity of the tree host species in each of the 54 combinations at the IDENT experiment in Montreal.

    Ab, Abies balsamea; Ap, Acer platanoides; Ar, Acer rubrum; As, Acer saccharum; Ba, Betula alleghaniensis; Bp, Betula papyrifera; Ld, Larix decidua; Ll, Larix laricina; Pa, Picea abies; Pg, Picea glauca; Po, Picea omorika; Pre, Pinus resinosa; Pru, Picea rubens; Pst, Pinus strobus; Psy, Pinus sylvestris; Qro, Quercus robur; Qru, Quercus rubra; Tc, Tilia cordata; To, Thuja occidentalis.

  4. Principal component analysis on functional traits community weighted means.
    Extended Data Fig. 2: Principal component analysis on functional traits community weighted means.

    Traits are: maximum photosynthetic capacity (Amass), nitrogen content of leaves (Nmass), leaf longevity (LL), wood density (WD) and leaf mass per area (LMA). Colours represent plot species richness levels (red for one species, orange for two, green for four, and blue for twelve).

  5. A priori structural equation model.
    Extended Data Fig. 3: A priori structural equation model.

    Factors are species richness, functional identity, functional diversity and plot microtopography (elevation at plot centre, cm) as determinants of leaf bacterial diversity and plant community productivity. Green boxes indicate exogenous variables (diversity indices and plot microtopography), whereas responses are in yellow for plot-level leaf bacterial diversity and blue for plant community productivity.

  6. Alternative structural equation model excluding the link between leaf bacterial diversity and plant community productivity.
    Extended Data Fig. 4: Alternative structural equation model excluding the link between leaf bacterial diversity and plant community productivity.

    After deletion of this link, the path analysis (n = 216, χ2 = 11.906, P = 0.008, df = 3; RMSEA = 0.00, P = 0.044) is unstable and inferior to the model with the leaf bacterial diversity–plant community productivity link included. Green boxes indicate plot-level plant diversity indices; yellow denotes plot-level leaf bacterial diversity; blue denotes plant community productivity. Numbers adjacent to arrows and arrow width indicate the effect size of the relationships and the associated bootstrap P value. +P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001. Continuous and dashed arrows indicate positive and negative relationships, respectively.

  7. Structural equation model of plant diversity and identity explaining leaf bacterial diversity and community composition, as well as plant community productivity (full model tested).
    Extended Data Fig. 5: Structural equation model of plant diversity and identity explaining leaf bacterial diversity and community composition, as well as plant community productivity (full model tested).

    Green boxes indicate plot-level plant diversity indices; yellow denotes plot-level leaf bacterial diversity; orange indicates plot-level leaf bacterial identity; blue denotes for plant community productivity. The covariances between leaf bacterial diversity and the two variables of leaf bacterial community composition were also included in the model.

  8. Structural equation model of plant diversity and identity explaining leaf bacterial diversity and community composition, as well as plant community productivity.
    Extended Data Fig. 6: Structural equation model of plant diversity and identity explaining leaf bacterial diversity and community composition, as well as plant community productivity.

    The path analysis (n = 216, χ2 = 1.522, P = 0.677, df = 3; RMSEA = 0.00, P = 0.821) explains 38% of the variance in leaf bacterial diversity, 34% and 11% of each components of bacterial identity, and 85% of the variance in plot productivity. Green boxes indicate plot-level plant diversity indices; yellow denotes plot-level leaf bacterial diversity; orange indicates plot-level leaf bacterial identity; blue denotes plant community productivity. Numbers adjacent to arrows and arrow width indicate the effect size of the relationships and the associated bootstrap P value. +P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001. Continuous and dashed arrows indicate positive and negative relationships, respectively. The covariances between leaf bacterial diversity and the two variables of leaf bacterial community composition were also included in the model.

Tables

  1. Host species functional traits
    Extended Data Table 1: Host species functional traits

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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

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 financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

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.

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

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: Identity of the tree host species in each of the 54 combinations at the IDENT experiment in Montreal. (104 KB)

    Ab, Abies balsamea; Ap, Acer platanoides; Ar, Acer rubrum; As, Acer saccharum; Ba, Betula alleghaniensis; Bp, Betula papyrifera; Ld, Larix decidua; Ll, Larix laricina; Pa, Picea abies; Pg, Picea glauca; Po, Picea omorika; Pre, Pinus resinosa; Pru, Picea rubens; Pst, Pinus strobus; Psy, Pinus sylvestris; Qro, Quercus robur; Qru, Quercus rubra; Tc, Tilia cordata; To, Thuja occidentalis.

  2. Extended Data Figure 2: Principal component analysis on functional traits community weighted means. (84 KB)

    Traits are: maximum photosynthetic capacity (Amass), nitrogen content of leaves (Nmass), leaf longevity (LL), wood density (WD) and leaf mass per area (LMA). Colours represent plot species richness levels (red for one species, orange for two, green for four, and blue for twelve).

  3. Extended Data Figure 3: A priori structural equation model. (211 KB)

    Factors are species richness, functional identity, functional diversity and plot microtopography (elevation at plot centre, cm) as determinants of leaf bacterial diversity and plant community productivity. Green boxes indicate exogenous variables (diversity indices and plot microtopography), whereas responses are in yellow for plot-level leaf bacterial diversity and blue for plant community productivity.

  4. Extended Data Figure 4: Alternative structural equation model excluding the link between leaf bacterial diversity and plant community productivity. (212 KB)

    After deletion of this link, the path analysis (n = 216, χ2 = 11.906, P = 0.008, df = 3; RMSEA = 0.00, P = 0.044) is unstable and inferior to the model with the leaf bacterial diversity–plant community productivity link included. Green boxes indicate plot-level plant diversity indices; yellow denotes plot-level leaf bacterial diversity; blue denotes plant community productivity. Numbers adjacent to arrows and arrow width indicate the effect size of the relationships and the associated bootstrap P value. +P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001. Continuous and dashed arrows indicate positive and negative relationships, respectively.

  5. Extended Data Figure 5: Structural equation model of plant diversity and identity explaining leaf bacterial diversity and community composition, as well as plant community productivity (full model tested). (248 KB)

    Green boxes indicate plot-level plant diversity indices; yellow denotes plot-level leaf bacterial diversity; orange indicates plot-level leaf bacterial identity; blue denotes for plant community productivity. The covariances between leaf bacterial diversity and the two variables of leaf bacterial community composition were also included in the model.

  6. Extended Data Figure 6: Structural equation model of plant diversity and identity explaining leaf bacterial diversity and community composition, as well as plant community productivity. (259 KB)

    The path analysis (n = 216, χ2 = 1.522, P = 0.677, df = 3; RMSEA = 0.00, P = 0.821) explains 38% of the variance in leaf bacterial diversity, 34% and 11% of each components of bacterial identity, and 85% of the variance in plot productivity. Green boxes indicate plot-level plant diversity indices; yellow denotes plot-level leaf bacterial diversity; orange indicates plot-level leaf bacterial identity; blue denotes plant community productivity. Numbers adjacent to arrows and arrow width indicate the effect size of the relationships and the associated bootstrap P value. +P < 0.1; *P < 0.05; **P < 0.01; ***P < 0.001. Continuous and dashed arrows indicate positive and negative relationships, respectively. The covariances between leaf bacterial diversity and the two variables of leaf bacterial community composition were also included in the model.

Extended Data Tables

  1. Extended Data Table 1: Host species functional traits (326 KB)

Additional data