Sensory Repertoire of Bacterial Chemoreceptors

Abstract

Chemoreceptors in bacteria detect a variety of signals and feed this information into chemosensory pathways that represent a major mode of signal transduction. The five chemoreceptors from Escherichia coli have served as traditional models in the study of this protein family. Genome analyses revealed that many bacteria contain much larger numbers of chemoreceptors with broader sensory capabilities. Chemoreceptors differ in topology, sensing mode, cellular location, and, above all, the type of ligand binding domain (LBD). Here, we highlight LBD diversity using well-established and emerging model organisms as well as genomic surveys. Nearly a hundred different types of protein domains that are found in chemoreceptor sequences are known or predicted LBDs, but only a few of them are ubiquitous. LBDs of the same class recognize different ligands, and conversely, the same ligand can be recognized by structurally different LBDs; however, recent studies began to reveal common characteristics in signal-LBD relationships. Although signals can stimulate chemoreceptors in a variety of different ways, diverse LBDs appear to employ a universal transmembrane signaling mechanism. Current and future studies aim to establish relationships between LBD types, the nature of signals that they recognize, and the mechanisms of signal recognition and transduction.

Keywords: chemotaxis; receptor-ligand interaction; signal transduction.

FIG 1

The chemoreceptor repertoires of E. coli, S. Typhimurium, and B. subtilis. Receptor topology, names, and locus tags of E. coli K-12, S. Typhimurium strain LT2, and Bacillus subtilis subsp. subtilis strain 168 are shown. The LBDs are colored and their type is annotated according to data in the Pfam database. Orthologous groups of chemoreceptors (including paralogs) are highlighted by blue shading.

FIG 2

The chemoreceptor repertoires of H. pylori and C. jejuni. Receptor topology and locus tags of H. pylori 26695 and C. jejuni subsp. jejuni NCTC 11168 are shown. Pfam names for all LBDs are shown, except for 4HB, which is predicted to be a divergent four-helix bundle domain. Domains that are not detected by the Pfam tool HMMER but are recognized by the more sensitive HHpred tool are indicated as empty rectangles. Orthologous groups of chemoreceptors (including paralogs) are highlighted by blue shading.

FIG 3

The chemoreceptor repertoires of three different Pseudomonas strains. Receptor topology and locus tags of P. aeruginosa PAO1, P. putida KT2440, and P. fluorescens Pf0-1 are shown. The LBDs are colored, and their type is annotated. Orthologous groups of chemoreceptors (including paralogs) are highlighted by blue shading. The question mark indicates a domain of an unknown type.

FIG 4

Relative abundances of different LBD types in chemoreceptors. The analysis includes sequences matching the chemoreceptor signaling domain (MCPsignal; Pfam accession number PF00015) that were available in the Pfam 31.0 database and its underlying UniProt reference proteome database (178) as of March 2017. See Table 4 for details.

FIG 5

Structural diversity of LBDs. Structures of different LBD types that are found in chemoreceptors are shown. Bound ligands are shown in red. Different chain colors indicate that the domain was experimentally shown to be dimeric. Domain definitions were obtained from Pfam. PDB accession numbers are shown in parentheses.

FIG 6

Diversity of ligands recognized by the major classes of chemoreceptor LBDs. The following ligands for which direct binding was observed are shown (along with references for the corresponding evidence): E. coli Tar (Ec-Tar) (63), Ec-Tsr (50), C. testosteroni MCP2901 (Ct-MCP2901) (203), Ct-MCP2983 (204), Ct-MCP2201 (40), P. aeruginosa CtpH (Pa-CtpH) (22, 141), P. putida McpS (Pp-McpS) (164), Pp-McpQ (167), H. pylori TlpB (Hp-TlpB) (97, 109), Pp-McpP (168), B. subtilis McpC (Bs-McpC) (89), Bs-McpB (9, 180), C. jejuni CcaA (Cj-CcaA) (116), Cj-CcmL (38, 179), Pa-PctA (138), Pa-PctB (138), Pp-McpA (163), V. cholerae Mlp37 (Vc-Mlp37) (44), Vc-Mlp24 (205), S. meliloti McpU (Sm-McpU) (206), Cj-Tlp11 (119), Pa-PctC (138), Pp-McpG (34), Sm-McpX (207), Pp-McpU (163), and Pp-McpH (162).

FIG 7

Different sensing mechanisms. (A to C) Sensing mechanism in which ligand binding induces LBD dimerization. (D and E) Sensing mechanism in which ligand binding does not induce LBD dimerization. (A and B) Zoomed-in images of the binding pockets of the Tar LBD (4HB) with bound Asp (PDB accession number 4Z9H) (A) and the McpS LBD (HBM) with malate (PDB accession number 2YFA) (B). The two monomers of the dimer are colored differently. In both cases, the binding site is at the dimer interface, and amino acids from both monomers are involved in ligand binding. (C) Analytical ultracentrifugation studies of the LBD of the McpS homolog McpQ (HBM) in the absence and presence of its ligand citrate. (D) Binding pocket of the dCache_1 LBD of the CcmL receptor (PDB accession number 4XMR) containing bound Ile. Amino acids involved in Ile binding are from the same monomer. (E) Analytical ultracentrifugation data for the PctA LBD (dCache_1) in the absence and presence of Ala. Data were reported previously (63, 138, 166, 167, 179). c(s), sedimentation coefficient distribution; AU, absorbance units; S, Svedberg units.

FIG 8

Diversity in signal recognition and modes of action. LBDs are shown in green.