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Genomics of cellular proliferation in periodic environmental fluctuations.

Jerome Salignon, Magali Richard, Etienne Fulcrand, Helene Duplus-Bottin, and Gael Yvert (2018)

Mol Syst Biol, 14(3):e7823.

Living systems control cell growth dynamically by processing information from their environment. Although responses to a single environmental change have beenintensively studied, little is known about how cells react to fluctuating conditions. Here, we address this question at the genomic scale by measuring therelative proliferation rate (fitness) of 3,568 yeast gene deletion mutants in out-of-equilibrium conditions: periodic oscillations between two environmental conditions. In periodic salt stress, fitness and its genetic variance largely depended on the oscillating period. Surprisingly, dozens of mutants displayed pronounced hyperproliferation under short stress periods, revealing unexpected controllers of growth under fast dynamics. We validated the implication of the high-affinity cAMP phosphodiesterase and of a regulator of protein translocationto mitochondria in this group. Periodic oscillations of extracellular methionine, a factor unrelated to salinity, also altered fitness but to a lesser extent and for different genes. The results illustrate how natural selection acts on mutations in a dynamic environment, highlighting unsuspected genetic vulnerabilities to periodic stress in molecular processes that are conserved across all eukaryotes.

 
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