IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-45897-6.html
   My bibliography  Save this article

Synthetic microbe-to-plant communication channels

Author

Listed:
  • Alice Boo

    (Massachusetts Institute of Technology)

  • Tyler Toth

    (Massachusetts Institute of Technology)

  • Qiguo Yu

    (Massachusetts Institute of Technology)

  • Alexander Pfotenhauer

    (University of Tennessee)

  • Brandon D. Fields

    (Massachusetts Institute of Technology)

  • Scott C. Lenaghan

    (University of Tennessee)

  • C. Neal Stewart

    (University of Tennessee)

  • Christopher A. Voigt

    (Massachusetts Institute of Technology)

Abstract

Plants and microbes communicate to collaborate to stop pests, scavenge nutrients, and react to environmental change. Microbiota consisting of thousands of species interact with each other and plants using a large chemical language that is interpreted by complex regulatory networks. In this work, we develop modular interkingdom communication channels, enabling bacteria to convey environmental stimuli to plants. We introduce a “sender device” in Pseudomonas putida and Klebsiella pneumoniae, that produces the small molecule p-coumaroyl-homoserine lactone (pC-HSL) when the output of a sensor or circuit turns on. This molecule triggers a “receiver device” in the plant to activate gene expression. We validate this system in Arabidopsis thaliana and Solanum tuberosum (potato) grown hydroponically and in soil, demonstrating its modularity by swapping bacteria that process different stimuli, including IPTG, aTc and arsenic. Programmable communication channels between bacteria and plants will enable microbial sentinels to transmit information to crops and provide the building blocks for designing artificial consortia.

Suggested Citation

  • Alice Boo & Tyler Toth & Qiguo Yu & Alexander Pfotenhauer & Brandon D. Fields & Scott C. Lenaghan & C. Neal Stewart & Christopher A. Voigt, 2024. "Synthetic microbe-to-plant communication channels," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45897-6
    DOI: 10.1038/s41467-024-45897-6
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-45897-6
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-45897-6?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. Subhayu Basu & Yoram Gerchman & Cynthia H. Collins & Frances H. Arnold & Ron Weiss, 2005. "A synthetic multicellular system for programmed pattern formation," Nature, Nature, vol. 434(7037), pages 1130-1134, April.
    2. Sonja Billerbeck & James Brisbois & Neta Agmon & Miguel Jimenez & Jasmine Temple & Michael Shen & Jef D. Boeke & Virginia W. Cornish, 2018. "A scalable peptide-GPCR language for engineering multicellular communication," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    3. Pei Du & Huiwei Zhao & Haoqian Zhang & Ruisha Wang & Jianyi Huang & Ye Tian & Xudong Luo & Xunxun Luo & Min Wang & Yanhui Xiang & Long Qian & Yihua Chen & Yong Tao & Chunbo Lou, 2020. "De novo design of an intercellular signaling toolbox for multi-channel cell–cell communication and biological computation," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    4. Amy L. Schaefer & E. P. Greenberg & Colin M. Oliver & Yasuhiro Oda & Jean J. Huang & Gili Bittan-Banin & Caroline M. Peres & Silke Schmidt & Katarina Juhaszova & Janice R. Sufrin & Caroline S. Harwood, 2008. "A new class of homoserine lactone quorum-sensing signals," Nature, Nature, vol. 454(7204), pages 595-599, July.
    5. Arianna Miano & Michael J. Liao & Jeff Hasty, 2020. "Inducible cell-to-cell signaling for tunable dynamics in microbial communities," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    6. Alvin Tamsir & Jeffrey J. Tabor & Christopher A. Voigt, 2011. "Robust multicellular computing using genetically encoded NOR gates and chemical ‘wires’," Nature, Nature, vol. 469(7329), pages 212-215, January.
    7. Barney A. Geddes & Ponraj Paramasivan & Amelie Joffrin & Amber L. Thompson & Kirsten Christensen & Beatriz Jorrin & Paul Brett & Stuart J. Conway & Giles E. D. Oldroyd & Philip S. Poole, 2019. "Engineering transkingdom signalling in plants to control gene expression in rhizosphere bacteria," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    8. Tal Danino & Octavio Mondragón-Palomino & Lev Tsimring & Jeff Hasty, 2010. "A synchronized quorum of genetic clocks," Nature, Nature, vol. 463(7279), pages 326-330, January.
    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. Singh, Vijai & Chaudhary, Dharmendra Kumar & Mani, Indra & Dhar, Pawan Kumar, 2016. "Recent advances and challenges of the use of cyanobacteria towards the production of biofuels," Renewable and Sustainable Energy Reviews, Elsevier, vol. 60(C), pages 1-10.
    2. Joaquín Gutiérrez Mena & Sant Kumar & Mustafa Khammash, 2022. "Dynamic cybergenetic control of bacterial co-culture composition via optogenetic feedback," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    3. Javier Macia & Romilde Manzoni & Núria Conde & Arturo Urrios & Eulàlia de Nadal & Ricard Solé & Francesc Posas, 2016. "Implementation of Complex Biological Logic Circuits Using Spatially Distributed Multicellular Consortia," PLOS Computational Biology, Public Library of Science, vol. 12(2), pages 1-24, February.
    4. Navneet Rai & Rajat Anand & Krishna Ramkumar & Varun Sreenivasan & Sugat Dabholkar & K V Venkatesh & Mukund Thattai, 2012. "Prediction by Promoter Logic in Bacterial Quorum Sensing," PLOS Computational Biology, Public Library of Science, vol. 8(1), pages 1-14, January.
    5. Masa Tsuchiya & Vincent Piras & Alessandro Giuliani & Masaru Tomita & Kumar Selvarajoo, 2010. "Collective Dynamics of Specific Gene Ensembles Crucial for Neutrophil Differentiation: The Existence of Genome Vehicles Revealed," PLOS ONE, Public Library of Science, vol. 5(8), pages 1-10, August.
    6. Onelia Gagliano & Camilla Luni & Yan Li & Silvia Angiolillo & Wei Qin & Francesco Panariello & Davide Cacchiarelli & Joseph S. Takahashi & Nicola Elvassore, 2021. "Synchronization between peripheral circadian clock and feeding-fasting cycles in microfluidic device sustains oscillatory pattern of transcriptome," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    7. Xianglai Li & Zhao Zhou & Wenna Li & Yajun Yan & Xiaolin Shen & Jia Wang & Xinxiao Sun & Qipeng Yuan, 2022. "Design of stable and self-regulated microbial consortia for chemical synthesis," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    8. Tai-Yin Chiu & Hui-Ju K Chiang & Ruei-Yang Huang & Jie-Hong R Jiang & François Fages, 2015. "Synthesizing Configurable Biochemical Implementation of Linear Systems from Their Transfer Function Specifications," PLOS ONE, Public Library of Science, vol. 10(9), pages 1-27, September.
    9. Zomorrodi, Ali R. & Maranas, Costas D., 2014. "Coarse-grained optimization-driven design and piecewise linear modeling of synthetic genetic circuits," European Journal of Operational Research, Elsevier, vol. 237(2), pages 665-676.
    10. Lukas Aufinger & Johann Brenner & Friedrich C. Simmel, 2022. "Complex dynamics in a synchronized cell-free genetic clock," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    11. Alex J. H. Fedorec & Neythen J. Treloar & Ke Yan Wen & Linda Dekker & Qing Hsuan Ong & Gabija Jurkeviciute & Enbo Lyu & Jack W. Rutter & Kathleen J. Y. Zhang & Luca Rosa & Alexey Zaikin & Chris P. Bar, 2024. "Emergent digital bio-computation through spatial diffusion and engineered bacteria," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    12. Lucas Henrion & Juan Andres Martinez & Vincent Vandenbroucke & Mathéo Delvenne & Samuel Telek & Andrew Zicler & Alexander Grünberger & Frank Delvigne, 2023. "Fitness cost associated with cell phenotypic switching drives population diversification dynamics and controllability," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Samanthe M Lyons & Wenlong Xu & June Medford & Ashok Prasad, 2014. "Loads Bias Genetic and Signaling Switches in Synthetic and Natural Systems," PLOS Computational Biology, Public Library of Science, vol. 10(3), pages 1-16, March.
    14. Brian D. Huang & Thomas M. Groseclose & Corey J. Wilson, 2022. "Transcriptional programming in a Bacteroides consortium," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    15. Emil D. Jensen & Marcus Deichmann & Xin Ma & Rikke U. Vilandt & Giovanni Schiesaro & Marie B. Rojek & Bettina Lengger & Line Eliasson & Justin M. Vento & Deniz Durmusoglu & Sandie P. Hovmand & Ibrahim, 2022. "Engineered cell differentiation and sexual reproduction in probiotic and mating yeasts," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. Volkov, Evgeny & Hellen, Edward H., 2021. "The effect of characteristic times on collective modes of two quorum sensing coupled identical ring oscillators," Chaos, Solitons & Fractals, Elsevier, vol. 151(C).
    17. John P. Marken & Richard M. Murray, 2023. "Addressable and adaptable intercellular communication via DNA messaging," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    18. Jung Hun Park & Gábor Holló & Yolanda Schaerli, 2024. "From resonance to chaos by modulating spatiotemporal patterns through a synthetic optogenetic oscillator," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    19. Guillermo Rodrigo & Santiago F Elena, 2011. "Structural Discrimination of Robustness in Transcriptional Feedforward Loops for Pattern Formation," PLOS ONE, Public Library of Science, vol. 6(2), pages 1-7, February.
    20. Karel Miettinen & Nattawat Leelahakorn & Aldo Almeida & Yong Zhao & Lukas R. Hansen & Iben E. Nikolajsen & Jens B. Andersen & Michael Givskov & Dan Staerk & Søren Bak & Sotirios C. Kampranis, 2022. "A GPCR-based yeast biosensor for biomedical, biotechnological, and point-of-use cannabinoid determination," Nature Communications, Nature, vol. 13(1), pages 1-16, 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:15:y:2024:i:1:d:10.1038_s41467-024-45897-6. 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.