Chemotactic signaling via carbohydrate phosphotransferase systems in Escherichia coli

Abstract

Chemotaxis allows bacteria to follow gradients of nutrients, environmental stimuli, and signaling molecules, optimizing bacterial growth and survival. Escherichia coli has long served as a model of bacterial chemotaxis, and the signal processing by the core of its chemotaxis pathway is well understood. However, most of the research so far has focused on one branch of chemotactic signaling, in which ligands bind to periplasmic sensory domains of transmembrane chemoreceptors and induce a conformational change that is transduced across the membrane to regulate activity of the receptor-associated kinase CheA. Here we quantitatively characterize another, receptor-independent branch of chemotactic signaling that is linked to the sugar uptake through a large family of phosphotransferase systems (PTSs). Using in vivo characterization of intracellular signaling and protein interactions, we demonstrate that signals from cytoplasmic PTS components are transmitted directly to the sensory complexes formed by chemoreceptors, CheA and an adapter protein CheW. We further conclude that despite different modes of sensing, the PTS- and receptor-mediated signals have similar regulatory effects on the conformation of the sensory complexes. As a consequence, both types of signals become integrated and undergo common downstream processing including methylation-dependent adaptation. We propose that such mode of signaling is essential for efficient chemotaxis to PTS substrates and may be common to most bacteria.

Dynamic Localization of a Transcription Factor in Bacillus subtilis: the LicT Antiterminator Relocalizes in Response to Inducer Availability

“…However, contradictory results have been reported for the localization of enzyme I in E. coli. Similar to our results, E. coli enzyme I was found to be distributed in the cytoplasm by Neumann et al (22), whereas a spotty distribution was reported by Patel et al (21). Finally, polar localization of enzyme I was observed by Lopian et al (20).…”

“…Recently, it has been suggested that the PTS is also spatially organized. Depending on the experimental setup and the growth conditions, the general PTS enzymes, EI and HPr, were found to localize to the cell poles, clustered in the cytoplasm or dispersed throughout the cell in E. coli (20,21,22). An even more complex spatiotemporal localization pattern was reported for the E. coli BglG protein, which controls the ␤-glucoside utilization genes in E. coli and is the functional counterpart of LicT.…”

Phosphotransferase protein EIIANtr interacts with SpoT, a key enzyme of the stringent response, in Ralstonia eutropha H16

“…The three domains of EII transporters may be fused or exist as independent proteins. The phosphorylation state of the PTS is sensed to coordinate various processes such as carbon catabolite repression, chemotaxis, biofilm formation or the activities of transcriptional regulators with carbohydrate availability (Deutscher, 2008;Görke & Stülke, 2008;Joyet et al, 2013;Neumann et al, 2012;Ymele-Leki et al, 2013). 2010; Powell et al, 1995).…”

Variation of swimming speed enhances the chemotactic migration of Escherichia coli

“…While detailed studies have focused on the molecular mechanism of sensing and adaptation via the Trg receptor (Hazelbauer and Engstrom 1980;Feng et al 1999;Li and Hazelbauer 2005), the latter is yet to be characterized in terms of the phenotypic response, namely, swimming speed and motor bias. In addition, glucose is also sensed through a PhosphoTransferase System (PTS) sugar uptake mechanism which operates in conjunction with the receptor mediated response through Trg (Adler and Epstein 1974;Lux et al 1995;Neumann et al 2012). Thus to study the response exclusively through the Trg receptor, we expose the two strains of cells, namely, wild type K12 and a mutant Dtrg, to varying concentrations and gradients of a non-metabolizable analogue of glucose, namely, 2-Deoxy-D-glucose (2Dg) (Adler and Epstein 1974).…”