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Mix of metabolites tunes root microbiota

Uncharacterized biosynthetic genes in plant genomes suggest that plants make a plethora of specialized metabolites. Huang et al. reconstructed three biosynthetic networks from the small mustard plant Arabidopsis thaliana. Promiscuous acyltransferases and dehydrogenases contributed to metabolite diversification. The plant may use these specialized metabolites to modulate the microbiota surrounding its roots. Disruption of the pathways and intervention with purified compounds caused changes in the root microbiota.
Science, this issue p. eaau6389

Structured Abstract

INTRODUCTION

Specialized metabolism is a feature of plant evolution and adaption. Plant-specialized metabolites have ecological functions, mediating interactions between plants and their environments. Although microbes can have diverse effects on plant growth and fitness, how plants assemble and modulate their microbiota remains unclear. Understanding the factors and mechanisms underlying this process will open up avenues for engineering plant microbiota for sustainable agriculture. Plants are estimated to use ~20% of their photosynthesized carbon to make root-derived organic molecules. However, whether (and if so, which) specialized metabolites can direct the assembly of specific root microbiota is not known.

RATIONALE

Triterpenes are plant-specialized metabolites that have functions in plant defense and signaling and also have antimicrobial activities. They are one of the largest and most structurally diverse families of plant natural products. The genome of the small mustard plant Arabidopsis thaliana harbors four root-expressed triterpene biosynthetic gene clusters that encode unknown triterpene biosynthetic pathways. Plant biosynthetic gene clustering is likely to be a result of strong selection pressure during evolution with associated production of small molecules of biological and ecological importance. Several of these clustered Arabidopsis genes have been implicated in defense against root pathogens, further suggesting that metabolites derived from these triterpene biosynthetic gene clusters may modulate the Arabidopsis root microbiota.

RESULTS

We have elucidated a specialized metabolic network expressed in the roots of A. thaliana that consists of functionally divergent triterpene biosynthetic gene clusters connected by scattered genes outside the clusters that encode promiscuous acyltransferases and alcohol dehydrogenases. This metabolic network has a latent capacity for synthesizing more than 50 previously unknown root metabolites. This is a relatively large number considering the total number of nonvolatile root metabolites that we detected (approximately 300). We characterized three divergent pathways for the biosynthesis of root triterpene metabolites: thalianin, thalianyl fatty acid esters, and arabidin. Analysis of the root microbiota of A. thaliana mutants disrupted in the biosynthesis of these compounds revealed shifts in the composition and diversity of their root microbiota compared with those of the wild type. Comparison with the root bacterial profiles of the taxonomically remote species rice and wheat supports a role for this specialized triterpene biosynthetic network in mediating the establishment of an Arabidopsis-specific microbiota. We next tested the activity of purified or synthesized Arabidopsis root triterpenes and representative triterpene cocktails in vitro toward 19 taxonomically diverse bacterial strains isolated from the A. thaliana root microbiota. We found that these compounds could indeed selectively modulate the growth of these bacteria, examples of both positive and negative modulation being evident. The modulation effects of the various triterpenes on the growth of different bacterial strains correlated with the relative differential abundance of the differential bacterial genera in the roots of A. thaliana Col-0 and triterpene mutant lines. Moreover, some root bacteria were found to be able to selectively metabolize certain triterpenes (such as thalianyl fatty acid esters) and use the breakdown products such as palmitic acid as carbon sources for proliferation.

CONCLUSION

We demonstrate that A. thaliana produces a range of specialized triterpenes that direct the assembly and maintenance of an A. thaliana–specific microbiota, enabling it to shape and tailor the microbial community within and around its roots to its own purposes. We speculate that metabolic diversification within the plant kingdom may provide a basis for communication and recognition that enables the sculpting of microbiota tailored to the needs of the host and that this may in part explain the existence of plant-specialized metabolism. Our study opens up opportunities for engineering root microbiota and further paves the way for investigating the functions of root microbiota in plant growth and health.
Dynamic modulation of the Arabidopsis root microbiota by specialized triterpene metabolites derived from biosynthetic gene clusters.
The specialized triterpenes thalianin, thalianyl fatty acid esters, and arabidin selectively modulate A. thaliana root microbiota members by promoting (indicated with the orange and purple bacteria) or inhibiting (indicated with the blue bacteria) the growth of different bacterial taxa and, in some cases, by serving as carbon sources (purple bacteria). These triterpenes are products of pathways encoded by biosynthetic gene clusters and nonclustered genes. Colored arrows indicate genes encoding different types of enzymes: black, triterpene synthase; red, cytochrome P450s; purple, acyltransferases; and blue, alcohol dehydrogenases. The dynamic modulation of root bacteria mediated by these specialized triterpenes contributes to the assembly of an A. thaliana–specific root microbiota.

Abstract

Plant specialized metabolites have ecological functions, yet the presence of numerous uncharacterized biosynthetic genes in plant genomes suggests that many molecules remain unknown. We discovered a triterpene biosynthetic network in the roots of the small mustard plant Arabidopsis thaliana. Collectively, we have elucidated and reconstituted three divergent pathways for the biosynthesis of root triterpenes, namely thalianin (seven steps), thalianyl medium-chain fatty acid esters (three steps), and arabidin (five steps). A. thaliana mutants disrupted in the biosynthesis of these compounds have altered root microbiota. In vitro bioassays with purified compounds reveal selective growth modulation activities of pathway metabolites toward root microbiota members and their biochemical transformation and utilization by bacteria, supporting a role for this biosynthetic network in shaping an Arabidopsis-specific root microbial community.

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Supplementary Material

Summary

Materials and Methods
Figs. S1 to S64
Tables S1 to S65
References (4660)

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Published In

Science
Volume 364 | Issue 6440
10 May 2019

Submission history

Received: 3 July 2018
Accepted: 25 March 2019
Published in print: 10 May 2019

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Acknowledgments

J. Pollier and P. Fernandez-Calvo are acknowledged for their support of Y-C.B.; C. Owen is acknowledged for initial testing of the thalianol cluster genes. Funding: This work has been supported by the National Institutes of Health Genome to Natural Products Network award U101GM110699 (A.O. and A.C.H.); the “Strategic Priority Research Program” of the Chinese Academy of Sciences (XDB11020700) (Y.B.); the Key Research Program of the Chinese Academy of Sciences (grant KFZD-SW-112-02-02, KFZD-SW-219) (Y.B.); the International Cooperation and Exchanges NSFC grant 31761143017 (Y.B.); the Centre of Excellence for Plant and Microbial Sciences (CEPAMS), established between the John Innes Centre and the Chinese Academy of Sciences and funded by the UK Biotechnology and Biological Sciences Research Council (BBSRC) and the Chinese Academy of Sciences (A.O. and Y.B.); the Priority Research Program of the Chinese Academy of Sciences (QYZDB-SSW-SMC021) (Y.B.); the European Community’s Seventh Framework Program (FP7/2007–2013) under grant agreement 613692 (TriForC) (A.O. and A.G.); the joint Engineering and Physical Sciences Research Council/ BBSRC-funded OpenPlant Synthetic Biology Research Centre grant BB/L014130/1 (H.-W.N., A.O.); and the Research Foundation Flanders with a research project grant to A.G. (G008417N). A.C.H. is supported by a European Commission Marie Skłodowska-Curie Individual Fellowship (H2020-MSCA-IF-EF-ST-702478-TRIGEM). H.-W.N. is currently supported by a Royal Society University Research Fellowship (UF160138). A.O.’s laboratory is funded by the UK BBSRC Institute Strategic Programme Grant “Molecules from Nature” (BB/P012523/1) and the John Innes Foundation. Y.-C.B. is supported by a China Scholarship Council (CSC) Ph.D. scholarship. Y.B. is supported by Thousand Youth Talents Plan (grant 2060299). Author contributions. A.C.H., Y. B., and A.O. conceived and designed the project. A.C.H. discovered and characterized the biosynthetic network, performed bacterial growth assay, and coordinated the project; T.J. grew plants in natural soils, harvested roots, prepared the 16S amplicon library for sequencing, isolated A. thaliana root bacteria and performed bacterial growth assays; Y.-X.L. performed bioinformatics analysis on microbiota sequencing results; Y.-C.B. generated the homozygous thaa1-crispr and thaa2-crispr lines; J.R. cloned the thalianol and marneral cluster genes; and B.Q. grew and harvested the wheat samples for microbiota analysis. A.C.H., T.J., Y.-X.L., H.-W.N., A.G., and Y.B. analyzed data; A.C.H., T.J., Y.B., and A.O. wrote the manuscript, with contributions from other authors. Competing interests: The authors declare that they have no competing interests. Data and materials availability: Raw microbiota sequencing data reported in this paper have been deposited in the Genome Sequence Archive in Beijing Institute of Genomics (BIG) Data Center (44), Chinese Academy of Sciences under accession no. PRJCA001296 that are public accessible at http://bigd.big.ac.cn/gsa. Scripts used in the microbiota analyses are available under the following link: https://github.com/microbiota/Huang2019SCIENCE.

Authors

Affiliations

Department of Metabolic Biology, John Innes Centre, Norwich Research Park, Colney Lane, Norwich NR4 7UH, UK.
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Science, Beijing, China.
CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences (CAS), Beijing 100101, China.
University of Chinese Academy of Sciences, College of Advanced Agricultural Sciences, Beijing 100039, China.
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Science, Beijing, China.
CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences (CAS), Beijing 100101, China.
Ghent University, Department of Plant Biotechnology and Bioinformatics, Ghent 9052, Belgium.
VIB Center for Plant Systems Biology, Ghent 9052, Belgium.
James Reed
Department of Metabolic Biology, John Innes Centre, Norwich Research Park, Colney Lane, Norwich NR4 7UH, UK.
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Science, Beijing, China.
CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences (CAS), Beijing 100101, China.
Ghent University, Department of Plant Biotechnology and Bioinformatics, Ghent 9052, Belgium.
VIB Center for Plant Systems Biology, Ghent 9052, Belgium.
Hans-Wilhelm Nützmann
Department of Metabolic Biology, John Innes Centre, Norwich Research Park, Colney Lane, Norwich NR4 7UH, UK.
Present address: Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK.
State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, Chinese Academy of Science, Beijing, China.
CAS-JIC Centre of Excellence for Plant and Microbial Science (CEPAMS), Institute of Genetics and Developmental Biology, Chinese Academy of Sciences (CAS), Beijing 100101, China.
University of Chinese Academy of Sciences, College of Advanced Agricultural Sciences, Beijing 100039, China.
Department of Metabolic Biology, John Innes Centre, Norwich Research Park, Colney Lane, Norwich NR4 7UH, UK.

Funding Information

European Commission: 613692 (TriForC)
Chinese Academy of Sciences: QYZDB-SSW-SMC021
Biotechnological and Biological Sciences Research Council (BBSRC): BB/P012523/1

Notes

*
These authors contributed equally to this work.
Corresponding author. Email: [email protected] (A.O.); [email protected] (Y.B.)

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