Abstract
Bacterial chemotaxis systems are as diverse as the environments that bacteria inhabit, but how much environmental variation can cells tolerate with a single system? Diversification of a single chemotaxis system could serve as an alternative, or even evolutionary stepping-stone, to switching between multiple systems. We hypothesized that mutations in gene regulation could lead to heritable control of chemotactic diversity. By simulating foraging and colonization of E. coli using a single-cell chemotaxis model, we found that different environments selected for different behaviors. The resulting trade-offs show that populations facing diverse environments would ideally diversify behaviors when time for navigation is limited. We show that advantageous diversity can arise from changes in the distribution of protein levels among individuals, which could occur through mutations in gene regulation. We propose experiments to test our prediction that chemotactic diversity in a clonal population could be a selectable trait that enables adaptation to environmental variability.DOI: http://dx.doi.org/10.7554/eLife.03526.001
Highlights
Escherichia coli uses a single chemotaxis protein network to navigate gradients of chemical attractants and repellents, as well as gradients of temperature, oxygen, and pH (Sourjik and Wingreen, 2012) (Figure 1A)
Due to the lack of quantitative information about the details of the natural environments of E. coli that would be relevant to chemotaxis, our goal is not the exact reconstruction of the distribution of challenges experienced by E. coli in the wild, but rather to use bacterial chemotaxis as a system to study the interactions between population diversity and environmental trade-offs
Using the definitions for adaptation time, clockwise bias, and CheY-P dynamic range, we reduced the molecular model into a phenotypic model written in terms of phenotypic parameters rather than protein levels (‘Materials and methods’)
Summary
Escherichia coli uses a single chemotaxis protein network to navigate gradients of chemical attractants and repellents, as well as gradients of temperature, oxygen, and pH (Sourjik and Wingreen, 2012) (Figure 1A). The core of the network is a two-component signal transduction system that carries chemical information gathered by transmembrane receptors to flagellar motors responsible for cell propulsion. While different receptors allow cells to sense different signals, all signals are processed through the same set of cytoplasmic proteins responsible for signal transduction and adaptation. This horizontal integration may impose conflicting demands on the regulation of these core decision-making components because signals can vary in time, space, and identity. We examine to what extent cell-to-cell variability in abundance of these core proteins may help resolve such conflicts
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