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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
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    References listed on IDEAS

    as
    1. 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.
    2. 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.
    3. 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.
    4. 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.
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