IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-43793-z.html
   My bibliography  Save this article

Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning

Author

Listed:
  • Barbara Emmenegger

    (ETH Zurich)

  • Julien Massoni

    (ETH Zurich)

  • Christine M. Pestalozzi

    (ETH Zurich)

  • Miriam Bortfeld-Miller

    (ETH Zurich)

  • Benjamin A. Maier

    (ETH Zurich)

  • Julia A. Vorholt

    (ETH Zurich)

Abstract

Plant-associated microbiomes contribute to important ecosystem functions such as host resistance to biotic and abiotic stresses. The factors that determine such community outcomes are inherently difficult to identify under complex environmental conditions. In this study, we present an experimental and analytical approach to explore microbiota properties relevant for a microbiota-conferred host phenotype, here plant protection, in a reductionist system. We screened 136 randomly assembled synthetic communities (SynComs) of five bacterial strains each, followed by classification and regression analyses as well as empirical validation to test potential explanatory factors of community structure and composition, including evenness, total commensal colonization, phylogenetic diversity, and strain identity. We find strain identity to be the most important predictor of pathogen reduction, with machine learning algorithms improving performances compared to random classifications (94-100% versus 32% recall) and non-modelled predictions (0.79-1.06 versus 1.5 RMSE). Further experimental validation confirms three strains as the main drivers of pathogen reduction and two additional strains that confer protection in combination. Beyond the specific application presented in our study, we provide a framework that can be adapted to help determine features relevant for microbiota function in other biological systems.

Suggested Citation

  • Barbara Emmenegger & Julien Massoni & Christine M. Pestalozzi & Miriam Bortfeld-Miller & Benjamin A. Maier & Julia A. Vorholt, 2023. "Identifying microbiota community patterns important for plant protection using synthetic communities and machine learning," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43793-z
    DOI: 10.1038/s41467-023-43793-z
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-43793-z
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-43793-z?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Zhong Wei & Tianjie Yang & Ville-Petri Friman & Yangchun Xu & Qirong Shen & Alexandre Jousset, 2015. "Trophic network architecture of root-associated bacterial communities determines pathogen invasion and plant health," Nature Communications, Nature, vol. 6(1), pages 1-9, December.
    2. Yang Bai & Daniel B. Müller & Girish Srinivas & Ruben Garrido-Oter & Eva Potthoff & Matthias Rott & Nina Dombrowski & Philipp C. Münch & Stijn Spaepen & Mitja Remus-Emsermann & Bruno Hüttel & Alice C., 2015. "Functional overlap of the Arabidopsis leaf and root microbiota," Nature, Nature, vol. 528(7582), pages 364-369, December.
    3. Jonathan S. Lefcheck & Graham J. Edgar & Rick D. Stuart-Smith & Amanda E. Bates & Conor Waldock & Simon J. Brandl & Stuart Kininmonth & Scott D. Ling & J. Emmett Duffy & Douglas B. Rasher & Aneil F. A, 2021. "Species richness and identity both determine the biomass of global reef fish communities," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    4. Junjie Qin & Ruiqiang Li & Jeroen Raes & Manimozhiyan Arumugam & Kristoffer Solvsten Burgdorf & Chaysavanh Manichanh & Trine Nielsen & Nicolas Pons & Florence Levenez & Takuji Yamada & Daniel R. Mende, 2010. "A human gut microbial gene catalogue established by metagenomic sequencing," Nature, Nature, vol. 464(7285), pages 59-65, March.
    5. Peter J. Turnbaugh & Ruth E. Ley & Micah Hamady & Claire M. Fraser-Liggett & Rob Knight & Jeffrey I. Gordon, 2007. "The Human Microbiome Project," Nature, Nature, vol. 449(7164), pages 804-810, October.
    6. Gabriel Castrillo & Paulo José Pereira Lima Teixeira & Sur Herrera Paredes & Theresa F. Law & Laura de Lorenzo & Meghan E. Feltcher & Omri M. Finkel & Natalie W. Breakfield & Piotr Mieczkowski & Corbi, 2017. "Root microbiota drive direct integration of phosphate stress and immunity," Nature, Nature, vol. 543(7646), pages 513-518, March.
    7. Isabelle Laforest-Lapointe & Alain Paquette & Christian Messier & Steven W. Kembel, 2017. "Leaf bacterial diversity mediates plant diversity and ecosystem function relationships," Nature, Nature, vol. 546(7656), pages 145-147, June.
    8. Peter J. Turnbaugh & Ruth E. Ley & Michael A. Mahowald & Vincent Magrini & Elaine R. Mardis & Jeffrey I. Gordon, 2006. "An obesity-associated gut microbiome with increased capacity for energy harvest," Nature, Nature, vol. 444(7122), pages 1027-1031, December.
    9. Omri M. Finkel & Isai Salas-González & Gabriel Castrillo & Jonathan M. Conway & Theresa F. Law & Paulo José Pereira Lima Teixeira & Ellie D. Wilson & Connor R. Fitzpatrick & Corbin D. Jones & Jeffery , 2020. "A single bacterial genus maintains root growth in a complex microbiome," Nature, Nature, vol. 587(7832), pages 103-108, November.
    10. Bates, Douglas & Mächler, Martin & Bolker, Ben & Walker, Steve, 2015. "Fitting Linear Mixed-Effects Models Using lme4," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 67(i01).
    11. Friedman, Jerome H. & Hastie, Trevor & Tibshirani, Rob, 2010. "Regularization Paths for Generalized Linear Models via Coordinate Descent," Journal of Statistical Software, Foundation for Open Access Statistics, vol. 33(i01).
    12. Michel Loreau & Andy Hector, 2001. "Partitioning selection and complementarity in biodiversity experiments," Nature, Nature, vol. 412(6842), pages 72-76, July.
    13. Michel Loreau & Andy Hector, 2001. "Erratum: Partitioning selection and complementarity in biodiversity experiments," Nature, Nature, vol. 413(6855), pages 548-548, October.
    14. Jonathan S. Lefcheck & Graham J. Edgar & Rick D. Stuart-Smith & Amanda E. Bates & Conor Waldock & Simon J. Brandl & Stuart Kininmonth & Scott D. Ling & J. Emmett Duffy & Douglas B. Rasher & Aneil F. A, 2021. "Publisher Correction: Species richness and identity both determine the biomass of global reef fish communities," Nature Communications, Nature, vol. 12(1), pages 1-1, December.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xin Zhou & Jinting Wang & Fang Liu & Junmin Liang & Peng Zhao & Clement K. M. Tsui & Lei Cai, 2022. "Cross-kingdom synthetic microbiota supports tomato suppression of Fusarium wilt disease," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    2. Shan Luo & Richard P. Phillips & Insu Jo & Songlin Fei & Jingjing Liang & Bernhard Schmid & Nico Eisenhauer, 2023. "Higher productivity in forests with mixed mycorrhizal strategies," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    3. Jian Lu & Raheel Ahmad & Thomas Nguyen & Jeffrey Cifello & Humza Hemani & Jiangyuan Li & Jinguo Chen & Siyi Li & Jing Wang & Achouak Achour & Joseph Chen & Meagan Colie & Ana Lustig & Christopher Dunn, 2022. "Heterogeneity and transcriptome changes of human CD8+ T cells across nine decades of life," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    4. Guangzhou Wang & Haley M. Burrill & Laura Y. Podzikowski & Maarten B. Eppinga & Fusuo Zhang & Junling Zhang & Peggy A. Schultz & James D. Bever, 2023. "Dilution of specialist pathogens drives productivity benefits from diversity in plant mixtures," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. Jonathan S. Lefcheck & Graham J. Edgar & Rick D. Stuart-Smith & Amanda E. Bates & Conor Waldock & Simon J. Brandl & Stuart Kininmonth & Scott D. Ling & J. Emmett Duffy & Douglas B. Rasher & Aneil F. A, 2021. "Species richness and identity both determine the biomass of global reef fish communities," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    6. Lauren P. Grant & Chris Gennings & Edmond P. Wickham & Derek Chapman & Shumei Sun & David C. Wheeler, 2018. "Modeling Pediatric Body Mass Index and Neighborhood Environment at Different Spatial Scales," IJERPH, MDPI, vol. 15(3), pages 1-19, March.
    7. Liting Zheng & Kathryn E. Barry & Nathaly R. Guerrero-Ramírez & Dylan Craven & Peter B. Reich & Kris Verheyen & Michael Scherer-Lorenzen & Nico Eisenhauer & Nadia Barsoum & Jürgen Bauhus & Helge Bruel, 2024. "Effects of plant diversity on productivity strengthen over time due to trait-dependent shifts in species overyielding," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    8. Yunjia Lai & Chih-Wei Liu & Yifei Yang & Yun-Chung Hsiao & Hongyu Ru & Kun Lu, 2021. "High-coverage metabolomics uncovers microbiota-driven biochemical landscape of interorgan transport and gut-brain communication in mice," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    9. Amirhossein Shamsaddini & Kimia Dadkhah & Patrick M Gillevet, 2020. "BiomMiner: An advanced exploratory microbiome analysis and visualization pipeline," PLOS ONE, Public Library of Science, vol. 15(6), pages 1-13, June.
    10. Sergei Schaub & Nadja El Benni, 2024. "How do price (risk) changes influence farmers’ preferences to reduce fertilizer application?," Agricultural Economics, International Association of Agricultural Economists, vol. 55(2), pages 365-383, March.
    11. Joshua P White & Simon Dennis & Martin Tomko & Jessica Bell & Stephan Winter, 2021. "Paths to social licence for tracking-data analytics in university research and services," PLOS ONE, Public Library of Science, vol. 16(5), pages 1-19, May.
    12. Jack S. Gisby & Norzawani B. Buang & Artemis Papadaki & Candice L. Clarke & Talat H. Malik & Nicholas Medjeral-Thomas & Damiola Pinheiro & Paige M. Mortimer & Shanice Lewis & Eleanor Sandhu & Stephen , 2022. "Multi-omics identify falling LRRC15 as a COVID-19 severity marker and persistent pro-thrombotic signals in convalescence," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    13. Huang, Wei & Manevska-Tasevska, Gordana & Hansson, Helena, 2024. "Does ecologization matter for technical efficiency in crop production? A case of Swedish agriculture," Land Use Policy, Elsevier, vol. 138(C).
    14. Heather E Wheeler & Kaanan P Shah & Jonathon Brenner & Tzintzuni Garcia & Keston Aquino-Michaels & GTEx Consortium & Nancy J Cox & Dan L Nicolae & Hae Kyung Im, 2016. "Survey of the Heritability and Sparse Architecture of Gene Expression Traits across Human Tissues," PLOS Genetics, Public Library of Science, vol. 12(11), pages 1-23, November.
    15. Gaia Molinaro & Irene Cogliati Dezza & Sarah Katharina Bühler & Christina Moutsiana & Tali Sharot, 2023. "Multifaceted information-seeking motives in children," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    16. Florian Pargent & Florian Pfisterer & Janek Thomas & Bernd Bischl, 2022. "Regularized target encoding outperforms traditional methods in supervised machine learning with high cardinality features," Computational Statistics, Springer, vol. 37(5), pages 2671-2692, November.
    17. Doris Vandeputte & Lindsey Commer & Raul Y. Tito & Gunter Kathagen & João Sabino & Séverine Vermeire & Karoline Faust & Jeroen Raes, 2021. "Temporal variability in quantitative human gut microbiome profiles and implications for clinical research," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    18. Zhu, Shuang-Guo & Tao, Hong-Yan & Li, Wen-Bo & Zhou, Rui & Gui, Yan-Wen & Zhu, Li & Zhang, Xiao-Lin & Wang, Wei & Wang, Bao-Zhong & Mei, Fu-Jian & Zhu, Hao & Xiong, You-Cai, 2023. "Phosphorus availability mediates plant–plant interaction and field productivity in maize-grass pea intercropping system: Field experiment and its global validation," Agricultural Systems, Elsevier, vol. 205(C).
    19. Yayu Wang & Xiaolin Wang & Shuai Sun & Canzhi Jin & Jianmu Su & Jinpu Wei & Xinyue Luo & Jiawen Wen & Tong Wei & Sunil Kumar Sahu & Hongfeng Zou & Hongyun Chen & Zhixin Mu & Gengyun Zhang & Xin Liu & , 2022. "GWAS, MWAS and mGWAS provide insights into precision agriculture based on genotype-dependent microbial effects in foxtail millet," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    20. Samuel E. Wuest & Lukas Schulz & Surbhi Rana & Julia Frommelt & Merten Ehmig & Nuno D. Pires & Ueli Grossniklaus & Christian S. Hardtke & Ulrich Z. Hammes & Bernhard Schmid & Pascal A. Niklaus, 2023. "Single-gene resolution of diversity-driven overyielding in plant genotype mixtures," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-43793-z. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.