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Killing by Type VI secretion drives clonal phase separation and the evolution of cooperation

Luke McNally, Eryn Bernardy, Jacob Thomas, Arben Kalziqi, Jennifer Pentz, Sam Brown, Brian Hammer, Peter J. Yunker, William Ratcliff
doi: https://doi.org/10.1101/063487
Luke McNally
1Centre for Immunity, Infection and Evolution, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
2Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Edinburgh EH9 3FL, UK
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Eryn Bernardy
3School of Biology, Georgia Institute of Technology. Atlanta, USA. 30332.
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Jacob Thomas
3School of Biology, Georgia Institute of Technology. Atlanta, USA. 30332.
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Arben Kalziqi
4School of Physics, Georgia Institute of Technology. Atlanta, GA, USA. 30332.
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Jennifer Pentz
3School of Biology, Georgia Institute of Technology. Atlanta, USA. 30332.
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Sam Brown
3School of Biology, Georgia Institute of Technology. Atlanta, USA. 30332.
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Brian Hammer
3School of Biology, Georgia Institute of Technology. Atlanta, USA. 30332.
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Peter J. Yunker
4School of Physics, Georgia Institute of Technology. Atlanta, GA, USA. 30332.
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  • For correspondence: ratcliff@gatech.edu peter.yunker@physics.gatech.edu
William Ratcliff
3School of Biology, Georgia Institute of Technology. Atlanta, USA. 30332.
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  • For correspondence: ratcliff@gatech.edu peter.yunker@physics.gatech.edu
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Summary

By nature of their small size, dense growth and frequent need for extracellular metabolism, microbes face persistent public goods dilemmas1–5. Spatial assortment can act as a general solution to social conflict by allowing extracellular goods to be utilized preferentially by productive genotypes1,6,7. Established mechanisms that generate microbial assortment depend on the availability of free space8–14; however, microbes often live in densely-packed environments, wherein these mechanisms are ineffective. Here, we describe a novel class of self-organized pattern formation that facilitates the development of spatial structure within densely-packed bacterial colonies. Contact-mediated killing through the Type VI secretion system (T6SS) drives high levels of assortment by precipitating phase separation, even in initially well-mixed populations that do not necessarily exhibit net growth. We examine these dynamics using three different classes of mathematical models and experiments with mutually antagonistic strains of Vibrio cholerae growing on solid media, and find that all appear to de-mix via the same ‘Model A’ universality class of order-disorder transition. We mathematically demonstrate that contact killing should favour the evolution of public goods cooperation, and empirically examine the relationship between T6SSs and potential cooperation through phylogenetic analysis. Across 26 genera of Proteobacteria and Bacteroidetes, the proportion of a strain’s genome that codes for potentially-exploitable secreted proteins increases significantly with boththe number of Type 6 secretion systems and the number of T6SS effectors that it possesses. This work demonstrates how antagonistic traits—likely evolved for the purpose of killing competitors—can indirectlylead to the evolution of cooperation by driving genetic phase separation.

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Posted July 14, 2016.
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Killing by Type VI secretion drives clonal phase separation and the evolution of cooperation
Luke McNally, Eryn Bernardy, Jacob Thomas, Arben Kalziqi, Jennifer Pentz, Sam Brown, Brian Hammer, Peter J. Yunker, William Ratcliff
bioRxiv 063487; doi: https://doi.org/10.1101/063487
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Killing by Type VI secretion drives clonal phase separation and the evolution of cooperation
Luke McNally, Eryn Bernardy, Jacob Thomas, Arben Kalziqi, Jennifer Pentz, Sam Brown, Brian Hammer, Peter J. Yunker, William Ratcliff
bioRxiv 063487; doi: https://doi.org/10.1101/063487

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