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Am Nat. 2011 Dec;178(6):E162-73. doi: 10.1086/662668. Epub 2011 Oct 26.

The evolution of bacteriocin production in bacterial biofilms.

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Program in Computational Biology, Memorial Sloan-Kettering Cancer Center, New York, New York 10065, USA.


Bacteriocin production is a spiteful behavior of bacteria that is central to the competitive dynamics of many human pathogens. Social evolution predicts that bacteriocin production is favored when bacteriocin-producing cells are mixed at intermediate frequency with their competitors and when competitive neighborhoods are localized. Both predictions are supported by biofilm experiments. However, the means by which physical and biological processes interact to produce conditions that favor the evolution of bacteriocin production remain to be investigated. Here we fill this gap using analytical and computational approaches. We identify and collapse key parameters into a single number, the critical bacteriocin range, that measures the threshold distance from a focal bacteriocin-producing cell within which its fitness is higher than that of a sensitive cell. We develop an agent-based model to test our predictions and confirm that bacteriocin production is most favored when relatedness is intermediate and competition is local. We then use invasion analysis to determine evolutionarily stable strategies for bacteriocin production. Finally, we perform long-term evolutionary simulations to analyze how the critical bacteriocin range and genetic lineage segregation affect biodiversity in multistrain biofilms. We find that biodiversity is maintained in highly segregated biofilms for a wide array of critical bacteriocin ranges. However, under conditions of high nutrient penetration leading to well-mixed biofilms, biodiversity rapidly decreases and becomes sensitive to the critical bacteriocin range.

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