Adaptability of non-genetic diversity in bacterial chemotaxis

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

eLife digest

Bacterial colonies are generally made up of genetically identical cells. Despite this, a closer look at the members of a bacterial colony shows that these cells can have very different behaviors. For example, some cells may grow more quickly than others, or be more resistant to antibiotics. The mechanisms driving this diversity are only beginning to be identified and understood.

Escherichia coli bacteria can move towards, or away from, certain chemicals in their surrounding environment to help them navigate toward favorable conditions. This behavior is known as chemotaxis. The signals from all of these chemicals are processed in E. coli by just one set of proteins, which control the different behaviors that are needed for the bacteria to follow them. Different numbers of these proteins are found in different—but genetically identical—bacteria, and the number of proteins is linked to how the bacteria perform these behaviors.

It has been suggested that diversity can be beneficial to the overall bacterial population, as it helps the population survive environmental changes. This suggests that the level of diversity in the population should adapt to the level of diversity in the environment. However, it remains unknown how this adaptation occurs.

Frankel et al. developed and combined several models and simulations to investigate whether differences in chemotaxis protein production help an E. coli colony to survive. The models show that in different environments, it can be beneficial for the population as a whole if different cells have different responses to the chemicals present. For example, if a lot of a useful chemical is present, bacteria are more likely to survive by heading straight to the source. If not much chemical is detected, the bacteria may need to move in a more exploratory manner.

Frankel et al. find that different amounts of chemotaxis proteins produce these different behaviors. To survive in a changing environment, it is therefore best for the E. coli colony to contain cells that have different amounts of these proteins. Frankel et al. propose that the variability of chemotaxis protein levels between genetically identical cells can change through mutations in the genes that control how many of the proteins are produced, and predict that such mutations allow populations to adapt to environmental changes.

The environments simulated in the model were much simpler than would be found in the real world, and Frankel et al. describe experiments that are now being performed to confirm and expand on their results. The model could be used in the future to shed light on the behavior of other cells that are genetically identical but exhibit diverse behaviors, from other bacterial species to more complex cancer cells.

DOI: http://dx.doi.org/10.7554/eLife.03526.002