Non-genetic diversity modulates population performance

Mol Syst Biol. 2016 Dec 19;12(12):895. doi: 10.15252/msb.20167044.

Abstract

Biological functions are typically performed by groups of cells that express predominantly the same genes, yet display a continuum of phenotypes. While it is known how one genotype can generate such non-genetic diversity, it remains unclear how different phenotypes contribute to the performance of biological function at the population level. We developed a microfluidic device to simultaneously measure the phenotype and chemotactic performance of tens of thousands of individual, freely swimming Escherichia coli as they climbed a gradient of attractant. We discovered that spatial structure spontaneously emerged from initially well-mixed wild-type populations due to non-genetic diversity. By manipulating the expression of key chemotaxis proteins, we established a causal relationship between protein expression, non-genetic diversity, and performance that was theoretically predicted. This approach generated a complete phenotype-to-performance map, in which we found a nonlinear regime. We used this map to demonstrate how changing the shape of a phenotypic distribution can have as large of an effect on collective performance as changing the mean phenotype, suggesting that selection could act on both during the process of adaptation.

Keywords: Jensen's inequality; cellular motility; chemotaxis; nonlinear systems; non‐genetic diversity.

MeSH terms

  • Adaptation, Physiological
  • Chemotaxis*
  • Escherichia coli / genetics
  • Escherichia coli / physiology*
  • Escherichia coli Proteins / metabolism*
  • Gene Expression Regulation, Bacterial
  • Microfluidic Analytical Techniques / instrumentation*
  • Models, Biological
  • Phenotype

Substances

  • Escherichia coli Proteins