Multiple functions of flagellar motility and chemotaxis in bacterial physiology

Abstract

Most swimming bacteria are capable of following gradients of nutrients, signaling molecules and other environmental factors that affect bacterial physiology. This tactic behavior became one of the most-studied model systems for signal transduction and quantitative biology, and underlying molecular mechanisms are well characterized in Escherichia coli and several other model bacteria. In this review, we focus primarily on less understood aspect of bacterial chemotaxis, namely its physiological relevance for individual bacterial cells and for bacterial populations. As evident from multiple recent studies, even for the same bacterial species flagellar motility and chemotaxis might serve multiple roles, depending on the physiological and environmental conditions. Among these, finding sources of nutrients and more generally locating niches that are optimal for growth appear to be one of the major functions of bacterial chemotaxis, which could explain many chemoeffector preferences as well as flagellar gene regulation. Chemotaxis might also generally enhance efficiency of environmental colonization by motile bacteria, which involves intricate interplay between individual and collective behaviors and trade-offs between growth and motility. Finally, motility and chemotaxis play multiple roles in collective behaviors of bacteria including swarming, biofilm formation and autoaggregation, as well as in their interactions with animal and plant hosts.

Keywords: Escherichia coli; chemotaxis; environmental adaptation; motility; physiology.

Figure 1.

Chemotactic behavior and signaling pathway. (A), Two prominent types of bacterial flagellar motility patterns, run-tumble and run-reverse-flick swimming. Both types of swimming lead to effective diffusion in homogeneous environments and get biased by the chemotaxis pathway to climb up physicochemical gradients. (B), Schematic representation of the chemotaxis pathway of E. coli, featuring clustered chemosensory complexes formed by receptors bound to histidine kinase CheA and adaptor protein CheW. Chemoreceptors detect chemical ligands, either directly via their ligand binding domains or indirectly upon interactions with periplasmic binding proteins (PBPs), and modulate activity of CheA. The signal is transmitted to flagellar motor by phosphorylation of the diffusible response regulator CheY, which modulates the direction of motor rotation. The signal is terminated by the phosphatase CheZ. Receptor methylation enzymes, the methyltransferase CheR and the methylesterase CheB carry out adaptation to steady stimulation and provide short-term memory for temporal concentration comparisons.

Figure 2.

Trade-offs in chemotactic behavior and regulation of chemotaxis. (A), Chemotactic response to time varying concentration profiles that could result from diffusive spreading of attractant patch needs to balance rapid gradient climbing and localization at the peak. Higher swimming velocity expands sensitivity range of bacterial chemotaxis, particularly in shallow gradients (right), but incurs additional energetic costs. (B), Motility and nutrient uptake are regulated antagonistically with biosynthetic machinery dependent on the nutritional quality of the carbon source. During growth in poor carbon sources (left), motility is upregulated in proportion to potentially higher advantage provided by chemotaxis towards sources of additional nutrients (search strategy). In rich carbon sources (right), motility is downregulated to enable higher investment into biosynthetic machinery (growth strategy).

Figure 3.

Collective chemotactic behaviors. (A), Population expansion driven by chemotaxis towards self-generated gradients produced by metabolite consumption in porous medium (left) results in a spatial organization of the cell population, with selection for motility at the front and for growth at the rear of the spreading colony (right). (B), Chemoattraction to quorum-sensing signals can enhance autoaggregation and biofilm formation in single or multi-species communities of bacteria that secrete an attractant. (C), Swirling collective motion emerges at high bacterial cell densities, as observed on maps of the local cell velocities (left). It impairs the chemotactic perception of gradients by inducing random reorientations on the time scale of gradient sensing (top right), thus reducing chemotactic drift above the cell density at which collective motion begin to emerge (bottom right, dashed line).

Figure 4.

Relevance of chemotactic motility in natural bacterial habitats. (A), In the gut, bacteria navigate in the lumen according to chemical gradients emanating from the epithelium. Motility is further used to penetrate the mucus layer that surrounds the epithelium. (B), In the rhizosphere, bacteria navigate through the complex structure of the soil and follow chemical gradients released by plant roots. (C), In the marine environment, bacteria follow chemical gradients released by planktonic and larger organisms and face turbulent flows which stir both the gradients and the cells as they swim.