Flagellar protein FliL: A many-splendored thing

Abstract

FliL is a bacterial flagellar protein demonstrated to associate with, and regulate ion flow through, the stator complex in a diverse array of bacterial species. FliL is also implicated in additional functions such as stabilizing the flagellar rod, modulating rotor bias, sensing the surface, and regulating gene expression. How can one protein do so many things? Its location is paramount to understanding its numerous functions. This review will look at the evidence, attempt to resolve some conflicting findings, and offer new thoughts on FliL.

Keywords: FliL; flagella; motor torque; rotor bias; stators; surface sensing; swarming; swimming.

FIGURE 1

Taxonomic prevalence of the FliL protein. Results of searching the HMMER database (Potter et al., 2018) using the FliL protein sequence from Escherichia coli (sourced from Ecocyc).

FIGURE 2

A model for FliL positioning at the flagella motor. Left: The bulk of the figure is derived from Mondino et al., 2022 (reproduced under the open access terms of the Creative Commons CC-BY license), where a complete representation of a bacterial flagellum was constructed using available high-resolution structures of subassemblies from several bacterial species, all drawn to scale (for full details, see Figure 1 in Mondino et al., 2022). In light of the recently published complete C-ring structures (see text), Mondino et al. (2022) kindly updated the C-ring in their figure using PDB 8T8O (Alejandro Buschiazzo, personal communication), shown here in its CCW orientation indicated by the black rightward-pointing arrows placed on the periplasmic RBM-3 domain of FliF. Also added was a schematic representation of FliF RBM-3 loops (red) that descend into the cytoplasm and interdigitate with the FliG (green) at the top of the C-ring. In Salmonella/Escherichia coli, FliL interacts with RBM-3 in both locations as highlighted by the green and red squares (see text). The “closed” configuration of the MotAB complex was rendered by repurposing the previously generated “open” complex (Mondino et al., 2022). The FliL supramolecular complex (magenta) is taken from (Guo & Liu, 2022), and positioned to surround the “open” stator complex that associates with the basal body; Borrelia FliL (178 residues) is similar in length to Salmonella FliL (154 residues) and folds similarly in Alphfold. Right: Rod subunits not visible in the image on the left are highlighted. IM, inner membrane; OM, outer membrane; PG, peptidoglycan.

FIGURE 3

Flagellar filaments from Salmonella enterica and Caulobacter crescentus severed within the rod. EM images of negatively stained filament-hook-rod structures from: (a) Wild-type (left) and ΔfliL (right) strains of Salmonella propagated on swarm medium (white bracket highlights curved hook). This panel is reproduced from (Attmannspacher et al., 2008) under the rights of re-use afforded the author. (b) A spontaneous Salmonella fliF (MS-ring) mutant propagated in viscous liquid medium. This panel is reproduced from (Okino et al., 1989) under ASM free use Creative Commons Attribution license. (c) Ejected flagella during developmental life cycle of C. crescentus. This panel is reproduced from (Kanbe et al., 2005), with republication permission obtained from the Copyright Clearance Center (license ID 1493052–1).