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A subcellular biochemical model for T6SS dynamics reveals winning competitive strategies

View ORCID ProfileYuexia Luna Lin, View ORCID ProfileStephanie N. Smith, View ORCID ProfileEva Kanso, View ORCID ProfileAlecia N. Septer, View ORCID ProfileChris H. Rycroft
doi: https://doi.org/10.1101/2021.07.17.452664
Yuexia Luna Lin
aJohn A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138
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  • ORCID record for Yuexia Luna Lin
Stephanie N. Smith
bDepartment of Earth, Marine, and Environmental Sciences, University of North Carolina, Chapel Hill, NC 27599
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  • ORCID record for Stephanie N. Smith
Eva Kanso
cDepartment of Aerospace and Mechanical Engineering, University of Southern California, Los Angeles, CA 90089-1191
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  • ORCID record for Eva Kanso
Alecia N. Septer
bDepartment of Earth, Marine, and Environmental Sciences, University of North Carolina, Chapel Hill, NC 27599
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  • ORCID record for Alecia N. Septer
  • For correspondence: alecia_septer@med.unc.edu chr@seas.harvard.edu
Chris H. Rycroft
aJohn A. Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, MA 02138
dComputational Research Division, Lawrence Berkeley Laboratory, Berkeley, CA 94720
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  • For correspondence: alecia_septer@med.unc.edu chr@seas.harvard.edu
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Abstract

The Type VI secretion system (T6SS) is a broadly distributed interbacterial weapon that can be used to eliminate competing bacterial populations. Although unarmed target populations are typically used to study T6SS function, bacteria most likely encounter other T6SS-armed competitors in nature. The outcome of such battles is not well understood, neither is the connection between the outcomes with the subcellular details of the T6SS. Here, we incorporated new biological data derived from natural competitors of Vibrio fischeri light organ symbionts to build a biochemical model for T6SS function at the single cell level. The model accounts for activation of structure formation, structure assembly, and deployment. By developing an integrated agent-based model (IABM) that incorporates strain-specific T6SS parameters, we replicated outcomes of biological competitions, validating our approach. We used the IABM to isolate and manipulate strain-specific physiological differences between competitors, in a way that is not possible using biological samples, to identify winning strategies for T6SS-armed populations. We found that a tipping point exists where the cost of building more T6SS weapons outweighs their protective ability. Furthermore, we found that competitions between a T6SS-armed population and a unarmed target had different outcomes dependent on the geometry of the battlefield: target cells survived at the edges of a range expansion scenario where unlimited territory could be claimed, while competitions within a confined space, much like the light organ crypts where natural V. fischeri compete, resulted in the rapid elimination of the unarmed competitor.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • https://github.com/ylunalin/BacSim-T6SS

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted July 17, 2021.
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A subcellular biochemical model for T6SS dynamics reveals winning competitive strategies
Yuexia Luna Lin, Stephanie N. Smith, Eva Kanso, Alecia N. Septer, Chris H. Rycroft
bioRxiv 2021.07.17.452664; doi: https://doi.org/10.1101/2021.07.17.452664
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A subcellular biochemical model for T6SS dynamics reveals winning competitive strategies
Yuexia Luna Lin, Stephanie N. Smith, Eva Kanso, Alecia N. Septer, Chris H. Rycroft
bioRxiv 2021.07.17.452664; doi: https://doi.org/10.1101/2021.07.17.452664

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