Evolution of a bistable genetic system in fluctuating and nonfluctuating environments

Author:

Fernández-Fernández Rocío1ORCID,Olivenza David R.2,Weyer Esther34,Singh Abhyudai34ORCID,Casadesús Josep2ORCID,Antonia Sánchez-Romero María1ORCID

Affiliation:

1. Departamento de Microbiología y Parasitología, Facultad de Farmacia, Universidad de Sevilla, Sevilla 41012, Spain

2. Departamento de Genética, Facultad de Biología, Universidad de Sevilla, Sevilla 41012, Spain

3. Department of Electrical and Computer Engineering, Center for Bioinformatics and Computational Biology, University of Delaware, Newark, DE 19716

4. Department of Biomedical Engineering, Center for Bioinformatics and Computational Biology, University of Delaware, Newark, DE 19716

Abstract

Epigenetic mechanisms can generate bacterial lineages capable of spontaneously switching between distinct phenotypes. Currently, mathematical models and simulations propose epigenetic switches as a mechanism of adaptation to deal with fluctuating environments. However, bacterial evolution experiments for testing these predictions are lacking. Here, we exploit an epigenetic switch in Salmonella enterica, the opvAB operon, to show clear evidence that OpvAB bistability persists in changing environments but not in stable conditions. Epigenetic control of transcription in the opvAB operon produces OpvAB OFF (phage-sensitive) and OpvAB ON (phage-resistant) cells in a reversible manner and may be interpreted as an example of bet-hedging to preadapt Salmonella populations to the encounter with phages. Our experimental observations and computational simulations illustrate the adaptive value of epigenetic variation as an evolutionary strategy for mutation avoidance in fluctuating environments. In addition, our study provides experimental support to game theory models predicting that phenotypic heterogeneity is advantageous in changing and unpredictable environments.

Funder

Ministerio de Ciencia e Innovación

Ministerio de Ciencia, Innovación y Universidades

HHS | NIH | National Institute of General Medical Sciences

Publisher

Proceedings of the National Academy of Sciences

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