Characterization of the Vibrio fischeri Fatty Acid Chemoreceptors, VfcB and VfcB2

Abstract

Bacteria use a wide variety of methyl-accepting chemotaxis proteins (MCPs) to mediate their attraction to or repulsion from different chemical signals in their environment. The bioluminescent marine bacterium Vibrio fischeri is the monospecific symbiont of the Hawaiian bobtail squid, Euprymna scolopes, and encodes a large repertoire of MCPs that are hypothesized to be used during different parts of its complex, multistage lifestyle. Here, we report the initial characterization of two such MCPs from V. fischeri that are responsible for mediating migration toward short-and medium-chain aliphatic (or fatty) acids. These receptors appear to be distributed among only members of the family Vibrionaceae and are likely descended from a receptor that has been lost by the majority of the members of this family. While chemotaxis greatly enhances the efficiency of host colonization by V. fischeri, fatty acids do not appear to be used as a chemical cue during this stage of the symbiosis. This study presents an example of straight-chain fatty acid chemoattraction and contributes to the growing body of characterized MCP-ligand interactions. F lagellar motility in bacteria is a complex, tightly regulated process. Through alternating cycles of swimming and tumbling, a bacterium is able to navigate its environment, either to move away from unfavorable conditions or to migrate toward a more favorable habitat (e.g., toward nutrient sources) (1, 2). This directed motility is termed chemotaxis and is mediated by the CheAY twocomponent signal transduction pathway. These proteins alter the relative time for which the flagellum rotates counterclockwise (CCW) or clockwise (CW) and, in turn, how much time the bacterium spends swimming or tumbling, respectively. This change in rotational direction is determined by the phosphorylation state of CheY, which is mediated primarily by membrane-bound receptors known as methyl-accepting chemotaxis proteins (MCPs). MCPs are ligand-binding sensory proteins and are generally embedded in the inner membrane with their ligand-binding domain (LBD) extended into the periplasm and their signaling domains present in the cytosol. Upon ligand binding, the MCP undergoes a conformational change that allows methylation of the signaling domain, thereby permitting a sensory signal to be transmitted across the inner membrane.Chemotaxis and MCPs have been most thoroughly studied in Escherichia coli, which encodes three to five distinct MCPs shown to be involved in the sensing of compounds such as amino acids, peptides, sugars, and electron acceptors (3-8). However, as the number of sequenced bacterial genomes grows, it has become apparent that many other bacteria contain much larger repertoires of MCPs (1). For example, the genome of Pseudomonas aeruginosa encodes 24 MCPs, that of Vibrio cholerae encodes 44, and that of Magnetospirillum magnetotacticum encodes the largest known set of 61 MCPs. Despite these large numbers of receptors, the number of known ligands is surprisingly small. Previous work has shown little ...

Pseudomonas aeruginosa responds to exogenous polyunsaturated fatty acids (PUFAs) by modifying phospholipid composition, membrane permeability, and phenotypes associated with virulence

“…Motility represents another phenotype associated with virulence in P. aeruginosa infections. Small molecules (e.g., fatty acids) are common mediators of bacterial behavior, such as chemotaxis and quorum sensing [ 39 – 41 ]. Furthermore, there have been many observed effects of fatty acids on bacterial motility [ 15 , 42 – 44 ].…”

Exogenous Polyunsaturated Fatty Acids Impact Membrane Remodeling and Affect Virulence Phenotypes among Pathogenic Vibrio Species

“…Symbols circled by a dotted line indicate significant differences (P Ͻ 0.002) compared to the control (no fatty acid) at the particular polymyxin B concentration. molecules, such as fatty acids, often serve as signals for chemotaxis and quorum sensing (41,42). Furthermore, the effects of fatty acids on bacterial motility have been documented (30,43).…”

A genomic comparison of 13 symbiotic Vibrio fischeri isolates from the perspective of their host source and colonization behavior

“…Among squid symbionts, nine of these MCP genes are specific to strain ES114 and, therefore, are unlikely to be critical for colonization; however, it is possible that their functions are compensated by non-homologous members of the other strains' MCP repertoires, thereby complicating any inference of their importance in light-organ colonization. Although some chemoattractants of V. fischeri have been identified, the specific ligands of the MCPs present in V. fischeri are known for only three (DeLoney-Marino et al, 2003;Brennan et al, 2013;Nikolakakis et al, 2015), none of which is required for light-organ colonization.…”