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Enzymatically-active bacterial microcompartments follow substrate gradients and are protected from aggregation in a cell-free system

View ORCID ProfileJan Steinkühler, Charlotte H. Abrahamson, Jaime Agudo-Canalejo, View ORCID ProfileRamin Golestanian, Danielle Tullman-Ercek, View ORCID ProfileNeha P. Kamat
doi: https://doi.org/10.1101/2022.05.16.492142
Jan Steinkühler
1Department of Biomedical Engineering, Northwestern University, Evanston, IL 60657
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  • ORCID record for Jan Steinkühler
  • For correspondence: nkamat@northwestern.edu ercek@northwestern.edu jan.steinkuehler@northwestern.edu
Charlotte H. Abrahamson
2Department of Chemical and Biological Engineering, Northwestern University, 9 Evanston, Illinois, USA
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Jaime Agudo-Canalejo
3Department of Living Matter Physics, Max Planck Institute for Dynamics and Self-Organization, D-37077 Göttingen, Germany
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Ramin Golestanian
3Department of Living Matter Physics, Max Planck Institute for Dynamics and Self-Organization, D-37077 Göttingen, Germany
4Rudolf Peierls Centre for Theoretical Physics, University of Oxford, Oxford OX1 3PU, United Kingdom
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Danielle Tullman-Ercek
2Department of Chemical and Biological Engineering, Northwestern University, 9 Evanston, Illinois, USA
5Center for Synthetic Biology, Northwestern University, Evanston, IL 60657
6Chemistry of Life Processes, Evanston, IL 60657
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  • For correspondence: nkamat@northwestern.edu ercek@northwestern.edu jan.steinkuehler@northwestern.edu
Neha P. Kamat
1Department of Biomedical Engineering, Northwestern University, Evanston, IL 60657
5Center for Synthetic Biology, Northwestern University, Evanston, IL 60657
6Chemistry of Life Processes, Evanston, IL 60657
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  • For correspondence: nkamat@northwestern.edu ercek@northwestern.edu jan.steinkuehler@northwestern.edu
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Abstract

The ability to dynamically control organelle movement and position is essential for cellular function. Yet the underlying mechanisms driving this organization have not been fully resolved. Here, we draw from recent experimental observations and theoretical models of enzyme chemotaxis to demonstrate the chemotaxis of a bacterial organelle, the 1,2 propanediol (1,2-PD) utilization bacterial microcompartment (MCP) from Salmonella enterica. Upon encapsulating MCPs in a cell-like, biomimetic compartment, we observed the directed movement of MCPs along an external gradient of substrate. Our analysis shows that MCPs not only chemotax towards their substrate but also that enzymatic activity and substrate turnover protect them against large-scale aggregation. Our results provide a first experimental demonstration of organelle chemotaxis in a synthetic cellular system and support a recent theoretical model of chemotaxis. Together this work reveals a potentially significant driver of organelle organization while contributing to the construction of synthetic cell-like materials.

Competing Interest Statement

The authors have declared no competing interest.

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Posted May 17, 2022.
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Enzymatically-active bacterial microcompartments follow substrate gradients and are protected from aggregation in a cell-free system
Jan Steinkühler, Charlotte H. Abrahamson, Jaime Agudo-Canalejo, Ramin Golestanian, Danielle Tullman-Ercek, Neha P. Kamat
bioRxiv 2022.05.16.492142; doi: https://doi.org/10.1101/2022.05.16.492142
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Enzymatically-active bacterial microcompartments follow substrate gradients and are protected from aggregation in a cell-free system
Jan Steinkühler, Charlotte H. Abrahamson, Jaime Agudo-Canalejo, Ramin Golestanian, Danielle Tullman-Ercek, Neha P. Kamat
bioRxiv 2022.05.16.492142; doi: https://doi.org/10.1101/2022.05.16.492142

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