Bacterial chemotaxis: information processing, thermodynamics, and behavior

Abstract

Escherichia coli has long been used as a model organism due to the extensive experimental characterization of its pathways and molecular components. Take chemotaxis as an example, which allows bacteria to sense and swim in response to chemicals, such as nutrients and toxins. Many of the pathway's remarkable sensing and signaling properties are now concisely summarized in terms of design (or engineering) principles. More recently, new approaches from information theory and stochastic thermodynamics have begun to address how pathways process environmental stimuli and what the limiting factors are. However, to fully capitalize on these theoretical advances, a closer connection with single-cell experiments will be required. IntroductionAll living organisms from animals to unicellular bacteria live under constant evolutionary pressure. To stay ahead in the game of evolution, organisms need to process noisy information, allowing them to make survival decisions quickly. However, to process information and move organisms also require energy. Thus the final behavior of any organism has to be an outcome which produces strong advantages under likely occurring environments. Chemotaxis of Escherichia coli is particularly well understood in terms of its molecular components, allowing this bacterium to migrate towards food and away from toxins [1][2][3][4][5]. Indeed, an ever increasing amount of studies has highlighted several design principles, i.e. engineering blue prints, ensuring exquisite sensitivity, efficiency, robustness, and wide dynamic range at all levels of the pathway.This review focuses on recent findings in E. coli chemotaxis, in particular on how molecular mechanisms give rise to information processing, its associated thermodynamic cost, and the resulting swimming behavior. What new design principles will be discovered next? Classical view of Escherichia coli chemotaxisEscherichia coli is a Gram-negative bacterium inhabiting soil, as well as the animal and human gastrointestinal tracts. Inside the host, it contributes to the digestion of food and enhances resistance against pathogens [6]. This bacterium has a relatively simple chemotactic pathway (Fig. 1 1A). External stimuli are processed at the receptor level, where receptors sense and memorize chemical concentrations from the past by their adapted methylation level (Fig. 1A, see red box for 'sensing module'). The receptor-signaling activity can be monitored experimentally by tagging the CheY and CheZ proteins with a fluorescence-resonance-energy-transfer (FRET) reporter pair to follow their phosphorylation-dependent interaction. To swim cells are equipped with 5-8 flagellar rotary motors (Fig. 1A, blue box for 'motility module'), each of which rotates either clockwise (CW) or counterclockwise (CCW). Taking together these flagella determine cell movement, given either by a 'run' or a random reorientation in a 'tumble' [7][8][9]. The phosphorylated protein CheY-p links sensing and motility (Fig. 1A). In absence of any chemical gradient E. coli per...

Optogenetic Manipulation of Cyclic Di-GMP (c-di-GMP) Levels Reveals the Role of c-di-GMP in Regulating Aerotaxis Receptor Activity in Azospirillum brasilense

“…During thermotaxis, E. coli cells do not simply move up or down a temperature gradient but sense a particular temperature, and this behavior depends on chemotaxis receptor activity, set by differential methylation (44,45). If aerotaxis is a form of precision sensing, then the accumulation of cells in the aerotactic band at a preferred position in the gradient is the result of the antagonistic signaling of receptors that sense oxygen (or a related cue such as redox) as an attractant versus those that sense oxygen as a repellent (or a related cue such as redox), with the summation of their signaling inputs ultimately determining the preferred position of the aerotaxis band in the gradient.…”

Borrelia burgdorferi CheD Promotes Various Functions in Chemotaxis and the Pathogenic Life Cycle of the Spirochete

“…The components of the chemotaxis signal transduction systems that mediate these responses are highly conserved among prokaryotes. The best-studied system is found in Escherichia coli (or Salmonella enterica serovar Typhimurium) (22)(23)(24). In this model organism, membrane-spanning methyl-accepting chemotaxis protein receptors (MCPs) detect environmental signals.…”

Functional Analysis of the Alternative Sigma-28 Factor FliA and Its Anti-Sigma Factor FlgM of the Nonflagellated Legionella Species L. oakridgensis

“…This was also true for loa2264, although we could not detect a sigma-28 consensus sequence in front of the gene (see below). Homologs of three of the fliA target genes (loa1456, loa0818, and loa2818) have been reported to also be fliA dependent in flagellated L. pneumophila strain Paris (14). A consensus sequence of fliA-dependent genes of L. pneumophila Corby was characterized earlier (see above) (8), and we screened the upstream region of FliA-dependent genes of L. oakridgensis for the presence of a similar consensus sequence.…”

“…Moreover, nonflagellated, nonmotile L. longbeachae species lack almost all genes of the flagellar regulon but have been shown to have a chemotaxis operon, and L. oakridgensis is negative for the flagellar regulon and the chemotaxis-encoding genes (4,10,11). In general, chemotaxis enables bacteria to locate special environmental conditions and get closer to higher concentrations of attractants (12)(13)(14). It will be interesting to further investigate the presence and role of chemotaxis genes in legionellae.…”