IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48295-0.html
   My bibliography  Save this article

A genetically encoded biosensor to monitor dynamic changes of c-di-GMP with high temporal resolution

Author

Listed:
  • Andreas Kaczmarczyk

    (University of Basel)

  • Simon Vliet

    (University of Basel)

  • Roman Peter Jakob

    (University of Basel)

  • Raphael Dias Teixeira

    (University of Basel)

  • Inga Scheidat

    (University of Basel)

  • Alberto Reinders

    (University of Basel)

  • Alexander Klotz

    (University of Basel)

  • Timm Maier

    (University of Basel)

  • Urs Jenal

    (University of Basel)

Abstract

Monitoring changes of signaling molecules and metabolites with high temporal resolution is key to understanding dynamic biological systems. Here, we use directed evolution to develop a genetically encoded ratiometric biosensor for c-di-GMP, a ubiquitous bacterial second messenger regulating important biological processes like motility, surface attachment, virulence and persistence. The resulting biosensor, cdGreen2, faithfully tracks c-di-GMP in single cells and with high temporal resolution over extended imaging times, making it possible to resolve regulatory networks driving bimodal developmental programs in different bacterial model organisms. We further adopt cdGreen2 as a simple tool for in vitro studies, facilitating high-throughput screens for compounds interfering with c-di-GMP signaling and biofilm formation. The sensitivity and versatility of cdGreen2 could help reveal c-di-GMP dynamics in a broad range of microorganisms with high temporal resolution. Its design principles could also serve as a blueprint for the development of similar, orthogonal biosensors for other signaling molecules, metabolites and antibiotics.

Suggested Citation

  • Andreas Kaczmarczyk & Simon Vliet & Roman Peter Jakob & Raphael Dias Teixeira & Inga Scheidat & Alberto Reinders & Alexander Klotz & Timm Maier & Urs Jenal, 2024. "A genetically encoded biosensor to monitor dynamic changes of c-di-GMP with high temporal resolution," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48295-0
    DOI: 10.1038/s41467-024-48295-0
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48295-0
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-024-48295-0?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. Dana C. Nadler & Stacy-Anne Morgan & Avi Flamholz & Kaitlyn E. Kortright & David F. Savage, 2016. "Rapid construction of metabolite biosensors using domain-insertion profiling," Nature Communications, Nature, vol. 7(1), pages 1-11, November.
    2. Andreas Kaczmarczyk & Antje M. Hempel & Christoph Arx & Raphael Böhm & Badri N. Dubey & Jutta Nesper & Tilman Schirmer & Sebastian Hiller & Urs Jenal, 2020. "Precise timing of transcription by c-di-GMP coordinates cell cycle and morphogenesis in Caulobacter," Nature Communications, Nature, vol. 11(1), pages 1-16, December.
    3. C. Lori & S. Ozaki & S. Steiner & R. Böhm & S. Abel & B. N. Dubey & T. Schirmer & S. Hiller & U. Jenal, 2015. "Cyclic di-GMP acts as a cell cycle oscillator to drive chromosome replication," Nature, Nature, vol. 523(7559), pages 236-239, July.
    4. Raphael D. Teixeira & Fabian Holzschuh & Tilman Schirmer, 2021. "Activation mechanism of a small prototypic Rec-GGDEF diguanylate cyclase," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. María Pérez-Burgos & Marco Herfurth & Andreas Kaczmarczyk & Andrea Harms & Katrin Huber & Urs Jenal & Timo Glatter & Lotte Søgaard-Andersen, 2024. "A deterministic, c-di-GMP-dependent program ensures the generation of phenotypically similar, symmetric daughter cells during cytokinesis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.

    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. Mitchell Brüderlin & Raphael Böhm & Firas Fadel & Sebastian Hiller & Tilman Schirmer & Badri N. Dubey, 2023. "Structural features discriminating hybrid histidine kinase Rec domains from response regulator homologs," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Zhong Guo & Oleh Smutok & Wayne A. Johnston & Patricia Walden & Jacobus P. J. Ungerer & Thomas S. Peat & Janet Newman & Jake Parker & Tom Nebl & Caryn Hepburn & Artem Melman & Richard J. Suderman & Ev, 2021. "Design of a methotrexate-controlled chemical dimerization system and its use in bio-electronic devices," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    3. Shuyu Li & Hengxi Sun & Jianghan Li & Yujiao Zhao & Ruiying Wang & Lei Xu & Chongyi Duan & Jialin Li & Zhuo Wang & Qinmeng Liu & Yao Wang & Songying Ouyang & Xihui Shen & Lei Zhang, 2022. "Autoinducer-2 and bile salts induce c-di-GMP synthesis to repress the T3SS via a T3SS chaperone," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Jin Wang & Ning Xue & Wenjia Pan & Ran Tu & Shixin Li & Yue Zhang & Yufeng Mao & Ye Liu & Haijiao Cheng & Yanmei Guo & Wei Yuan & Xiaomeng Ni & Meng Wang, 2023. "Repurposing conformational changes in ANL superfamily enzymes to rapidly generate biosensors for organic and amino acids," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Michael B. Sheets & Nathan Tague & Mary J. Dunlop, 2023. "An optogenetic toolkit for light-inducible antibiotic resistance," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Liyuan Zhu & Harold M. McNamara & Jared E. Toettcher, 2023. "Light-switchable transcription factors obtained by direct screening in mammalian cells," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    7. Willow Coyote-Maestas & David Nedrud & Antonio Suma & Yungui He & Kenneth A. Matreyek & Douglas M. Fowler & Vincenzo Carnevale & Chad L. Myers & Daniel Schmidt, 2021. "Probing ion channel functional architecture and domain recombination compatibility by massively parallel domain insertion profiling," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    8. Dorothy Koveal & Paul C. Rosen & Dylan J. Meyer & Carlos Manlio Díaz-García & Yongcheng Wang & Li-Heng Cai & Peter J. Chou & David A. Weitz & Gary Yellen, 2022. "A high-throughput multiparameter screen for accelerated development and optimization of soluble genetically encoded fluorescent biosensors," Nature Communications, Nature, vol. 13(1), pages 1-14, 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_s41467-024-48295-0. 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.