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Molecular basis and design principles of switchable front-rear polarity and directional migration in Myxococcus xanthus

Author

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  • Luís António Menezes Carreira

    (Max Planck Institute for Terrestrial Microbiology)

  • Dobromir Szadkowski

    (Max Planck Institute for Terrestrial Microbiology)

  • Stefano Lometto

    (Evolutionary Biochemistry Group, Max Planck Institute for Terrestrial Microbiology
    Philipps University)

  • Georg. K. A. Hochberg

    (Evolutionary Biochemistry Group, Max Planck Institute for Terrestrial Microbiology
    Philipps University)

  • Lotte Søgaard-Andersen

    (Max Planck Institute for Terrestrial Microbiology)

Abstract

During cell migration, front-rear polarity is spatiotemporally regulated; however, the underlying design of regulatory interactions varies. In rod-shaped Myxococcus xanthus cells, a spatial toggle switch dynamically regulates front-rear polarity. The polarity module establishes front-rear polarity by guaranteeing front pole-localization of the small GTPase MglA. Conversely, the Frz chemosensory system, by acting on the polarity module, causes polarity inversions. MglA localization depends on the RomR/RomX GEF and MglB/RomY GAP complexes that localize asymmetrically to the poles by unknown mechanisms. Here, we show that RomR and the MglB and MglC roadblock domain proteins generate a positive feedback by forming a RomR/MglC/MglB complex, thereby establishing the rear pole with high GAP activity that is non-permissive to MglA. MglA at the front engages in negative feedback that breaks the RomR/MglC/MglB positive feedback allosterically, thus ensuring low GAP activity at this pole. These findings unravel the design principles of a system for switchable front-rear polarity.

Suggested Citation

  • Luís António Menezes Carreira & Dobromir Szadkowski & Stefano Lometto & Georg. K. A. Hochberg & Lotte Søgaard-Andersen, 2023. "Molecular basis and design principles of switchable front-rear polarity and directional migration in Myxococcus xanthus," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39773-y
    DOI: 10.1038/s41467-023-39773-y
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    2. Luís António Menezes Carreira & Filipe Tostevin & Ulrich Gerland & Lotte Søgaard-Andersen, 2020. "Protein-protein interaction network controlling establishment and maintenance of switchable cell polarity," PLOS Genetics, Public Library of Science, vol. 16(6), pages 1-30, June.
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    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.

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