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Bacterial chemotaxis represents one of the simplest and best studied examples of unicellular behavior. Chemotaxis allows swimming bacterial cells to follow chemical gradients in the environment by performing temporal comparisons of ligand concentrations. The process of chemotaxis in the model bacterium Escherichia coli has been studied in great molecular detail over the past 40 years, using a large range of experimental tools to investigate physiology, genetics and biochemistry of the system. The abundance of quantitative experimental data enabled detailed computational modeling of the pathway and theoretical analyses of such properties as robustness and signal amplification. Because of the temporal mode of gradient sensing in bacterial chemotaxis, molecular memory is an essential component of the chemotaxis pathway. Recent studies suggest that the memory time scale has been evolutionary optimized to perform optimal comparisons of stimuli while swimming in the gradient. Moreover, noise in the adaptation system, which results from variations of the adaptation rate both over time and among cells, might be beneficial for the overall chemotactic performance of the population.

Chemotaxis allows bacteria to colonize their environment more efficiently and to find optimal growth conditions, and is consequently under strong evolutionary selection. Theoretical and experimental analyses of bacterial chemotaxis suggested that the pathway has been evolutionarily optimized to produce robust output under conditions of such physiological perturbations as stochastic intercellular variations in protein levels while at the same time minimizing complexity and cost of protein expression. Pathway topology in Escherichia coli apparently evolved to produce an invariant output under concerted variations in protein levels, consistent with experimentally observed transcriptional coupling of chemotaxis genes. Here, we show that the pathway robustness is further enhanced through the pairwise translational coupling of adjacent genes. Computer simulations predicted that the robustness of the pathway against the uncorrelated variations in protein levels can be enhanced by a selective pairwise coupling of individual chemotaxis genes on one mRNA, with the order of genes in E. coli ranking among the best in terms of noise compensation. Translational coupling between chemotaxis genes was experimentally confirmed, and coupled expression of these genes was shown to improve chemotaxis. Bioinformatics analysis further revealed that E. coli gene order corresponds to consensus in sequenced bacterial genomes, confirming evolutionary selection for noise reduction. Since polycistronic gene organization is common in bacteria, translational coupling between adjacent genes may provide a general mechanism to enhance robustness of their signaling and metabolic networks. Moreover, coupling between expression of neighboring genes is also present in eukaryotes, and similar principles of noise reduction might thus apply to all cellular networks. [ABSTRACT FROM AUTHOR]