Bacterial amino acid chemotaxis: a widespread strategy with multiple physiological and ecological roles

Abstract

Chemotaxis is the directed, flagellum-based movement of bacteria in chemoeffector gradients. Bacteria respond chemotactically to a wide range of chemoeffectors, including amino, organic, and fatty acids, sugars, polyamines, quaternary amines, purines, pyrimidines, aromatic hydrocarbons, oxygen, inorganic ions, or polysaccharides. Most frequent are chemotactic responses to amino acids (AAs), which were observed in numerous bacteria regardless of their phylogeny and lifestyle. Mostly chemoattraction responses are observed, although a number of bacteria are repelled from certain AAs. Chemoattraction is associated with the important metabolic value of AAs as growth substrates or building blocks of proteins. However, additional studies revealed that AAs are also sensed as environmental cues. Many chemoreceptors are specific for AAs, and signaling is typically initiated by direct ligand binding to their four-helix bundle or dCache ligand-binding domains. Frequently, bacteria possess multiple AA-responsive chemoreceptors that at times possess complementary AA ligand spectra. The identification of sequence motifs in the binding sites at dCache_1 domains has permitted to define an AA-specific family of dCache_1AA chemoreceptors. In addition, AAs are among the ligands recognized by broad ligand range chemoreceptors, and evidence was obtained for chemoreceptor activation by the binding of AA-loaded solute-binding proteins. The biological significance of AA chemotaxis is very ample including in biofilm formation, root and seed colonization by beneficial bacteria, plant entry of phytopathogens, colonization of the intestine, or different virulence-related features in human/animal pathogens. This review provides insights that may be helpful for the study of AA chemotaxis in other uncharacterized bacteria.

Keywords: amino acid; chemotaxis; signal transduction.

Fig 1

Scheme of the repellent chemotaxis response to D-amino acids in V. cholerae. In response to starvation (or other stress conditions), the sigma factor RpoS induces the expression of the mcp_DRK-bsrV operon, which encodes the chemoreceptor MCP_DRK and the racemase BsrV. The MCP_DRK receptor recognizes D-Arg and D-Lys at its 4HB-type LBD, triggering a chemorepellent response. Figure adapted from reference (39).

Fig 2

Amino acid recognition at chemoreceptors. (A) 3D structures of Tar-LBD (S. enterica sv. Typhimurium) in complex with L-Asp (pdb ID 1vlt) and PctA-LBD (P. aeruginosa) in complex with L-Trp (pdb ID 5t7m), (B) superimposition of Tar-LBD/L-Asp with MCP_DRK-LBD (V. cholerae) with the bound chemorepellent D-Arg (pdb ID 8bsa), and (C) AlphaFold2 (49) models of Halobacterium salinarum BasT-LBD and the BasB solute-binding protein (in complex with L-Leu).

Fig 3

Sequence alignment of the PctA, PctB, and PctC chemoreceptors of P. aeruginosa PAO1. Amino acids in red are identical, in green strongly similar, and in blue weakly similar. tm: transmembrane. The alignment was made using the MUSCLE protein sequence alignment tool of NPSA (79) using default settings.

Fig 4

The dCache_1AA family for the recognition of amino acids. (A) Zoom at the binding pocket of the PctA chemoreceptor containing bound L-Trp (yellow). The amino acids of the AA binding motif are shown in red (interaction with the carboxylate group) and blue (interaction with the amino group). (B) Protein sequence alignment of experimentally studied bacterial dCache_1 domains with respective ligands. The AA-binding motif (shaded in blue and red) is present in all AA-binding dCache_1 domains (gray background). (C) The AA-binding motif across the Tree of Life. Thick lines with dots at the tips denote the presence of the AA-binding motif. Figure modified from reference (81), with permission.

Fig 5

The multiple physiological and ecological functions of chemotaxis to amino acids in bacteria. Schematic representation of the role of AA chemotaxis for access to nutrients, colonization and infection of hosts, co-transport of non-motile microorganisms (microbial hitchhiking), and biofilm formation.