IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39773-y.html
   My bibliography  Save this article

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

Author

Listed:
  • 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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39773-y
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-39773-y?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. Sandrine Etienne-Manneville & Alan Hall, 2002. "Rho GTPases in cell biology," Nature, Nature, vol. 420(6916), pages 629-635, December.
    2. Adar Sonn-Segev & Katarina Belacic & Tatyana Bodrug & Gavin Young & Ryan T. VanderLinden & Brenda A. Schulman & Johannes Schimpf & Thorsten Friedrich & Phat Vinh Dip & Thomas U. Schwartz & Benedikt Ba, 2020. "Quantifying the heterogeneity of macromolecular machines by mass photometry," Nature Communications, Nature, vol. 11(1), pages 1-10, December.
    3. 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.
    4. Anja Spang & Jimmy H. Saw & Steffen L. Jørgensen & Katarzyna Zaremba-Niedzwiedzka & Joran Martijn & Anders E. Lind & Roel van Eijk & Christa Schleper & Lionel Guy & Thijs J. G. Ettema, 2015. "Complex archaea that bridge the gap between prokaryotes and eukaryotes," Nature, Nature, vol. 521(7551), pages 173-179, May.
    5. Christian Galicia & Sébastien Lhospice & Paloma Fernández Varela & Stefano Trapani & Wenhua Zhang & Jorge Navaza & Julien Herrou & Tâm Mignot & Jacqueline Cherfils, 2019. "MglA functions as a three-state GTPase to control movement reversals of Myxococcus xanthus," Nature Communications, Nature, vol. 10(1), pages 1-12, December.
    6. John Jumper & Richard Evans & Alexander Pritzel & Tim Green & Michael Figurnov & Olaf Ronneberger & Kathryn Tunyasuvunakool & Russ Bates & Augustin Žídek & Anna Potapenko & Alex Bridgland & Clemens Me, 2021. "Highly accurate protein structure prediction with AlphaFold," Nature, Nature, vol. 596(7873), pages 583-589, August.
    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. Leonardo Betancurt-Anzola & Markel Martínez-Carranza & Marc Delarue & Kelly M. Zatopek & Andrew F. Gardner & Ludovic Sauguet, 2023. "Molecular basis for proofreading by the unique exonuclease domain of Family-D DNA polymerases," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Gabriela Casanova-Sepúlveda & Joel A. Sexton & Benjamin E. Turk & Titus J. Boggon, 2023. "Autoregulation of the LIM kinases by their PDZ domain," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Clément Madru & Markel Martínez-Carranza & Sébastien Laurent & Alessandra C. Alberti & Maelenn Chevreuil & Bertrand Raynal & Ahmed Haouz & Rémy A. Meur & Marc Delarue & Ghislaine Henneke & Didier Flam, 2023. "DNA-binding mechanism and evolution of replication protein A," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    4. Yuan Lin & Theresa A. Ramelot & Simge Senyuz & Attila Gursoy & Hyunbum Jang & Ruth Nussinov & Ozlem Keskin & Yi Zheng, 2024. "Tumor-derived RHOA mutants interact with effectors in the GDP-bound state," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    5. Xiuling Wu & Yanhe Zhao & Hong Zhang & Wendi Yang & Jinbo Yang & Lifang Sun & Meiqin Jiang & Qin Wang & Qianchao Wang & Xianren Ye & Xuewu Zhang & Yunkun Wu, 2023. "Mechanism of regulation of the Helicobacter pylori Cagβ ATPase by CagZ," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. John C. K. Wang & Hannah T. Baddock & Amirhossein Mafi & Ian T. Foe & Matthew Bratkowski & Ting-Yu Lin & Zena D. Jensvold & Magdalena Preciado López & David Stokoe & Dan Eaton & Qi Hao & Aaron H. Nile, 2024. "Structure of the p53 degradation complex from HPV16," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    7. Elena Ethel Vidal-Calvo & Anne Martin-Salazar & Swati Choudhary & Robert Dagil & Sai Sundar Rajan Raghavan & Lara Duvnjak & Mie Anemone Nordmaj & Thomas Mandel Clausen & Ann Skafte & Jan Oberkofler & , 2024. "Tumor-agnostic cancer therapy using antibodies targeting oncofetal chondroitin sulfate," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    8. 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.
    9. Marios G. Koliopoulos & Reyhan Muhammad & Theodoros I. Roumeliotis & Fabienne Beuron & Jyoti S. Choudhary & Claudio Alfieri, 2022. "Structure of a nucleosome-bound MuvB transcription factor complex reveals DNA remodelling," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    10. Jithesh Kottur & Radhika Malik & Aneel K. Aggarwal, 2024. "Nucleic acid mediated activation of a short prokaryotic Argonaute immune system," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    11. Tomoyuki Hatano & Saravanan Palani & Dimitra Papatziamou & Ralf Salzer & Diorge P. Souza & Daniel Tamarit & Mehul Makwana & Antonia Potter & Alexandra Haig & Wenjue Xu & David Townsend & David Rochest, 2022. "Asgard archaea shed light on the evolutionary origins of the eukaryotic ubiquitin-ESCRT machinery," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    12. Ye Yuan & Lei Chen & Kexu Song & Miaomiao Cheng & Ling Fang & Lingfei Kong & Lanlan Yu & Ruonan Wang & Zhendong Fu & Minmin Sun & Qian Wang & Chengjun Cui & Haojue Wang & Jiuyang He & Xiaonan Wang & Y, 2024. "Stable peptide-assembled nanozyme mimicking dual antifungal actions," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    13. Ivica Odorčić & Mohamed Belal Hamed & Sam Lismont & Lucía Chávez-Gutiérrez & Rouslan G. Efremov, 2024. "Apo and Aβ46-bound γ-secretase structures provide insights into amyloid-β processing by the APH-1B isoform," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Léon Faure & Bastien Mollet & Wolfram Liebermeister & Jean-Loup Faulon, 2023. "A neural-mechanistic hybrid approach improving the predictive power of genome-scale metabolic models," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    15. Tian Zhu & Merry H. Ma, 2022. "Deriving the Optimal Strategy for the Two Dice Pig Game via Reinforcement Learning," Stats, MDPI, vol. 5(3), pages 1-14, August.
    16. Stella Vitt & Simone Prinz & Martin Eisinger & Ulrich Ermler & Wolfgang Buckel, 2022. "Purification and structural characterization of the Na+-translocating ferredoxin: NAD+ reductase (Rnf) complex of Clostridium tetanomorphum," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    17. Pierre Azoulay & Joshua Krieger & Abhishek Nagaraj, 2024. "Old Moats for New Models: Openness, Control, and Competition in Generative AI," NBER Chapters, in: Entrepreneurship and Innovation Policy and the Economy, volume 4, National Bureau of Economic Research, Inc.
    18. Riya Shah & Thomas C. Panagiotou & Gregory B. Cole & Trevor F. Moraes & Brigitte D. Lavoie & Christopher A. McCulloch & Andrew Wilde, 2024. "The DIAPH3 linker specifies a β-actin network that maintains RhoA and Myosin-II at the cytokinetic furrow," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    19. Yashan Yang & Qianqian Shao & Mingcheng Guo & Lin Han & Xinyue Zhao & Aohan Wang & Xiangyun Li & Bo Wang & Ji-An Pan & Zhenguo Chen & Andrei Fokine & Lei Sun & Qianglin Fang, 2024. "Capsid structure of bacteriophage ΦKZ provides insights into assembly and stabilization of jumbo phages," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    20. Anthony C. Bishop & Glorisé Torres-Montalvo & Sravya Kotaru & Kyle Mimun & A. Joshua Wand, 2023. "Robust automated backbone triple resonance NMR assignments of proteins using Bayesian-based simulated annealing," Nature Communications, Nature, vol. 14(1), pages 1-15, 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_s41467-023-39773-y. 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.