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A synthetic communication system uncovers self-jamming of bacteriophage transmission

View ORCID ProfileAmit Pathania, Corbin Hopper, View ORCID ProfileAmir Pandi, Matthias Függer, View ORCID ProfileThomas Nowak, View ORCID ProfileManish Kushwaha
doi: https://doi.org/10.1101/2022.05.11.491355
Amit Pathania
1Université Paris-Saclay, INRAe, AgroParisTech, Micalis Institute, 78352 Jouy-en-Josas, France
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Corbin Hopper
1Université Paris-Saclay, INRAe, AgroParisTech, Micalis Institute, 78352 Jouy-en-Josas, France
2Université Paris-Saclay, CNRS, ENS Paris-Saclay, Laboratoire Méthodes Formelles, Inria, 91190 Gif-sur-Yvette, France
3Université Paris-Saclay, CNRS, Laboratoire Interdisciplinaire des Sciences du Numérique, 91405 Orsay, France
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Amir Pandi
1Université Paris-Saclay, INRAe, AgroParisTech, Micalis Institute, 78352 Jouy-en-Josas, France
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Matthias Függer
2Université Paris-Saclay, CNRS, ENS Paris-Saclay, Laboratoire Méthodes Formelles, Inria, 91190 Gif-sur-Yvette, France
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  • For correspondence: mfuegger@lsv.fr thomas.nowak@lri.fr manish.kushwaha@inrae.fr
Thomas Nowak
3Université Paris-Saclay, CNRS, Laboratoire Interdisciplinaire des Sciences du Numérique, 91405 Orsay, France
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  • For correspondence: mfuegger@lsv.fr thomas.nowak@lri.fr manish.kushwaha@inrae.fr
Manish Kushwaha
1Université Paris-Saclay, INRAe, AgroParisTech, Micalis Institute, 78352 Jouy-en-Josas, France
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  • For correspondence: mfuegger@lsv.fr thomas.nowak@lri.fr manish.kushwaha@inrae.fr
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Abstract

Intercellular communication enables coordinated action by cells of microbial communities and multicellular organisms, often mediated by molecular exchange of information. Inspired by their success, synthetic biologists have recently started implementing population-level controls in engineered organisms with the aim of expanding circuit size and complexity. Yet, realising the true potential of multicellular synthetic biology requires an expanded communication alphabet as well as quantitative models to predict complex behaviour. Towards that aim, here we repurpose the M13 bacteriophage machinery for cell-to-cell communication between Escherichia coli cells and characterise the signalling dynamics. The fitted quantitative model includes the growth burden of the communication machinery, the relationship between cellular growth phase and the secretion-infection kinetics, and concurrent antibiotic selection. Limitations of deterministic models are demonstrated, with stochastic effects playing a key role in reproducing the observed infection kinetics. Surprisingly, we discover that the M13 minor coat protein pIII is released into the medium to confer extracellular immunity to uninfected cells. In a simulated gut environment, this mechanism enables the phage to farm uninfected bacterial cells for the future, increasing the overall success of both M13 and E. coli. In addition to establishing a tool for intercellular communication, our work uncovers the mutualistic nature of a phage-bacterial relationship that has evolved over long-term coexistence.

Competing Interest Statement

The authors have declared no competing interest.

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 May 11, 2022.
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A synthetic communication system uncovers self-jamming of bacteriophage transmission
Amit Pathania, Corbin Hopper, Amir Pandi, Matthias Függer, Thomas Nowak, Manish Kushwaha
bioRxiv 2022.05.11.491355; doi: https://doi.org/10.1101/2022.05.11.491355
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A synthetic communication system uncovers self-jamming of bacteriophage transmission
Amit Pathania, Corbin Hopper, Amir Pandi, Matthias Függer, Thomas Nowak, Manish Kushwaha
bioRxiv 2022.05.11.491355; doi: https://doi.org/10.1101/2022.05.11.491355

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