Leaf bacterial diversity mediates plant diversity and ecosystem function relationships

Research on biodiversity and ecosystem functioning has demonstrated links between plant diversity and ecosystem functions such as productivity. At other trophic levels, the plant microbiome has been shown to influence host plant fitness and function, and host-associated microbes have been proposed to influence ecosystem function through their role in defining the extended phenotype of host organisms 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.

[1]  S. Lindow,et al.  Contribution of Indole-3-Acetic Acid Production to the Epiphytic Fitness of Erwinia herbicola , 1998, Applied and Environmental Microbiology.

[2]  Campbell O. Webb,et al.  Picante: R tools for integrating phylogenies and ecology , 2010, Bioinform..

[3]  Sean C. Thomas,et al.  The worldwide leaf economics spectrum , 2004, Nature.

[4]  P. Reich,et al.  Functional identity is the main driver of diversity effects in young tree communities. , 2016, Ecology letters.

[5]  William A. Walters,et al.  QIIME allows analysis of high-throughput community sequencing data , 2010, Nature Methods.

[6]  S. Hubbell,et al.  Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest , 2014, Proceedings of the National Academy of Sciences.

[7]  P. Legendre,et al.  A distance-based framework for measuring functional diversity from multiple traits. , 2010, Ecology.

[8]  W. Cho,et al.  Bacterial communities in the phylloplane of Prunus species , 2015, Journal of basic microbiology.

[9]  C. Pieterse,et al.  Modulation of host immunity by beneficial microbes. , 2012, Molecular plant-microbe interactions : MPMI.

[10]  Dana L. Carper,et al.  Evidence for foliar endophytic nitrogen fixation in a widely distributed subalpine conifer. , 2016, The New phytologist.

[11]  C. Pieterse,et al.  The rhizosphere microbiome and plant health. , 2012, Trends in plant science.

[12]  Michel Loreau,et al.  From selection to complementarity: shifts in the causes of biodiversity–productivity relationships in a long-term biodiversity experiment , 2007, Proceedings of the Royal Society B: Biological Sciences.

[13]  Eoin L. Brodie,et al.  Greengenes, a Chimera-Checked 16S rRNA Gene Database and Workbench Compatible with ARB , 2006, Applied and Environmental Microbiology.

[14]  C. Messier,et al.  Host species identity, site and time drive temperate tree phyllosphere bacterial community structure , 2016, Microbiome.

[15]  J. Chave,et al.  Towards a Worldwide Wood Economics Spectrum 2 . L E a D I N G D I M E N S I O N S I N W O O D F U N C T I O N , 2022 .

[16]  Daniel B. Müller,et al.  The Plant Microbiota: Systems-Level Insights and Perspectives. , 2016, Annual review of genetics.

[17]  L. Falquet,et al.  The microbiome of the leaf surface of Arabidopsis protects against a fungal pathogen. , 2016, The New phytologist.

[18]  Shahid Naeem,et al.  Functional and phylogenetic diversity as predictors of biodiversity--ecosystem-function relationships. , 2011, Ecology.

[19]  Detlef Weigel,et al.  Microbial Hub Taxa Link Host and Abiotic Factors to Plant Microbiome Variation , 2016, PLoS biology.

[20]  Xiangming Xu,et al.  Dispersal of Bacillus subtilis and its effect on strawberry phyllosphere microbiota under open field and protection conditions , 2016, Scientific Reports.

[21]  J. Vorholt.  Microbial life in the phyllosphere , 2012, Nature Reviews Microbiology.

[22]  C. V. Mering,et al.  Metaproteogenomic analysis of microbial communities in the phyllosphere and rhizosphere of rice , 2011, The ISME Journal.

[23]  Michel Loreau,et al.  Partitioning selection and complementarity in biodiversity experiments , 2001, Nature.

[24]  Rob Knight,et al.  The ecology of the phyllosphere: geographic and phylogenetic variability in the distribution of bacteria on tree leaves. , 2010, Environmental microbiology.

[25]  Korbinian Strimmer,et al.  APE: Analyses of Phylogenetics and Evolution in R language , 2004, Bioinform..

[26]  Ü. Niinemets,et al.  Tolerance to shade, drought, and waterlogging of temperate northern hemisphere trees and shrubs , 2006 .

[27]  S. Lindow,et al.  Heterogeneous transcription of an indoleacetic acid biosynthetic gene in Erwinia herbicola on plant surfaces , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[28]  Jiajie Zhang,et al.  PEAR: a fast and accurate Illumina Paired-End reAd mergeR , 2013, Bioinform..

[29]  Shinichi Nakagawa,et al.  A general and simple method for obtaining R2 from generalized linear mixed‐effects models , 2013 .

[30]  Filippo Bussotti,et al.  Positive biodiversity-productivity relationship predominant in global forests , 2016, Science.

[31]  Philippe Vandenkoornhuyse,et al.  The importance of the microbiome of the plant holobiont. , 2015, The New phytologist.

[32]  Fabien Quétier,et al.  Assessing functional diversity in the field - methodology matters! , 2007 .

[33]  Patrick L. Thompson,et al.  A general biodiversity–function relationship is mediated by trophic level , 2017 .

[34]  Forest Isbell,et al.  Biodiversity impacts ecosystem productivity as much as resources, disturbance, or herbivory , 2012, Proceedings of the National Academy of Sciences.

[35]  Paul C. Johnson.  Extension of Nakagawa & Schielzeth's R2GLMM to random slopes models , 2014, Methods in ecology and evolution.

[36]  E. Borer,et al.  Anthropogenic environmental changes affect ecosystem stability via biodiversity , 2015, Science.

[37]  P. Reich,et al.  Advancing biodiversity–ecosystem functioning science using high-density tree-based experiments over functional diversity gradients , 2013, Oecologia.

[38]  F. Bringel,et al.  Pivotal roles of phyllosphere microorganisms at the interface between plant functioning and atmospheric trace gas dynamics , 2015, Front. Microbiol..

[39]  Robert C. Edgar,et al.  BIOINFORMATICS APPLICATIONS NOTE , 2001 .

[40]  M. Loreau,et al.  Tropical tree diversity enhances light capture through crown plasticity and spatial and temporal niche differences , 2014 .

[41]  Dominique Gravel,et al.  Trophic complementarity drives the biodiversity-ecosystem functioning relationship in food webs. , 2013, Ecology letters.

[42]  J. Lennon,et al.  Rapid responses of soil microorganisms improve plant fitness in novel environments , 2012, Proceedings of the National Academy of Sciences.

[43]  J. Vorholt,et al.  A Synthetic Community Approach Reveals Plant Genotypes Affecting the Phyllosphere Microbiota , 2014, PLoS genetics.

[44]  Jacques Ravel,et al.  An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform , 2014, Microbiome.

[45]  Michel Loreau,et al.  Contributions of a global network of tree diversity experiments to sustainable forest plantations , 2015, Ambio.

[46]  Martin Schaefer,et al.  Land use intensification alters ecosystem multifunctionality via loss of biodiversity and changes to functional composition , 2015, Ecology letters.

[47]  M. Henn,et al.  A Novel Microbiome Therapeutic Increases Gut Microbial Diversity and Prevents Recurrent Clostridium difficile Infection. , 2016, The Journal of infectious diseases.