Self-organization of mortal filaments and its role in bacterial division ring formation

Vanhille-Campos CE, Whitley KD, Radler P, Loose M, Holden S, Šarić A. 2024. Self-organization of mortal filaments and its role in bacterial division ring formation. Nature Physics.

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Corresponding author has ISTA affiliation

Abstract
Filaments in the cell commonly treadmill. Driven by energy consumption, they grow on one end while shrinking on the other, causing filaments to appear motile even though individual proteins remain static. This process is characteristic of cytoskeletal filaments and leads to collective filament self-organization. Here we show that treadmilling drives filament nematic ordering by dissolving misaligned filaments. Taking the bacterial FtsZ protein involved in cell division as an example, we show that this mechanism aligns FtsZ filaments in vitro and drives the organization of the division ring in living Bacillus subtilis cells. We find that ordering via local dissolution also allows the system to quickly respond to chemical and geometrical biases in the cell, enabling us to quantitatively explain the ring formation dynamics in vivo. Beyond FtsZ and other cytoskeletal filaments, our study identifies a mechanism for self-organization via constant birth and death of energy-consuming filaments.
Publishing Year
Date Published
2024-08-12
Journal Title
Nature Physics
Publisher
Springer Nature
Acknowledgement
We thank I. Palaia (ISTA) for useful discussions and K. Lim and R. W. Wong (WPI-Nano Life Science Institute, Kanazawa University) for providing access to HS-AFM. We would like to thank B. Prats Mateu (MSD Austria, Vienna) for providing the HS-AFM data. This work was supported by the Royal Society (grant no. UF160266; C.V.-C. and A.Š.), the European Union’s Horizon 2020 Research and Innovation Programme (grant no. 802960; A.Š.), the Austrian Science Fund (FWF) Stand-Alone P34607 (M.L.) and a Wellcome Trust and Royal Society Sir Henry Dale Fellowship (grant no. 206670/Z/17/Z; S.H. and K.D.W.).
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IST-REx-ID

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Vanhille-Campos CE, Whitley KD, Radler P, Loose M, Holden S, Šarić A. Self-organization of mortal filaments and its role in bacterial division ring formation. Nature Physics. 2024. doi:10.1038/s41567-024-02597-8
Vanhille-Campos, C. E., Whitley, K. D., Radler, P., Loose, M., Holden, S., & Šarić, A. (2024). Self-organization of mortal filaments and its role in bacterial division ring formation. Nature Physics. Springer Nature. https://doi.org/10.1038/s41567-024-02597-8
Vanhille-Campos, Christian Eduardo, Kevin D. Whitley, Philipp Radler, Martin Loose, Séamus Holden, and Anđela Šarić. “Self-Organization of Mortal Filaments and Its Role in Bacterial Division Ring Formation.” Nature Physics. Springer Nature, 2024. https://doi.org/10.1038/s41567-024-02597-8.
C. E. Vanhille-Campos, K. D. Whitley, P. Radler, M. Loose, S. Holden, and A. Šarić, “Self-organization of mortal filaments and its role in bacterial division ring formation,” Nature Physics. Springer Nature, 2024.
Vanhille-Campos CE, Whitley KD, Radler P, Loose M, Holden S, Šarić A. 2024. Self-organization of mortal filaments and its role in bacterial division ring formation. Nature Physics.
Vanhille-Campos, Christian Eduardo, et al. “Self-Organization of Mortal Filaments and Its Role in Bacterial Division Ring Formation.” Nature Physics, Springer Nature, 2024, doi:10.1038/s41567-024-02597-8.
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