Construction and Loss of Bacterial Flagellar Filaments

Abstract

The bacterial flagellar filament is an extracellular tubular protein structure that acts as a propeller for bacterial swimming motility. It is connected to the membrane-anchored rotary bacterial flagellar motor through a short hook. The bacterial flagellar filament consists of approximately 20,000 flagellins and can be several micrometers long. In this article, we reviewed the experimental works and models of flagellar filament construction and the recent findings of flagellar filament ejection during the cell cycle. The length-dependent decay of flagellar filament growth data supports the injection-diffusion model. The decay of flagellar growth rate is due to reduced transportation of long-distance diffusion and jamming. However, the filament is not a permeant structure. Several bacterial species actively abandon their flagella under starvation. Flagellum is disassembled when the rod is broken, resulting in an ejection of the filament with a partial rod and hook. The inner membrane component is then diffused on the membrane before further breakdown. These new findings open a new field of bacterial macro-molecule assembly, disassembly, and signal transduction.

Keywords: flagellar ejection; injection-diffusion model; self-assembly.

Figure 1

Bacterial flagellar motors are mainly classified into proton-driven and sodium-driven motors. Torque generation requires an interaction between stator units and FliG on the C-ring. In the proton-driven motor of E. coli, the stator is composed of MotA and MotB, whereas PomA and PomB are sodium-driven analogues in V. alginolyticus. The common elements for both motor types are LP, MS, and C rings. In V. alginolyticus, an additional sheath covers the flagellar filament.

Figure 2

Schematic of vT3SS and fT3SS. The vT3SS and fT3SS are similar in terms of cytoplasmic components and the inner membrane export apparatus. ATPase associates with proteins to pump unfolded substrates into the export channel. Then, the sorting platform and export gate help line up the sequence of unfolded substrates. The flagellum consists of a rod, hook structure, and flagellar filament. The needle connects with rings to directly pass through the outer membrane.

Figure 3

A timeline of experiments and models on flagellar filament construction and loss.

Figure 4

Potential mechanisms of the flagellar growth process. (A) Schematics of the chain model (left) and the injection-diffusion model (right) are shown. The chain model proposed that sequential flagellins are linked head-to-tail to form a chain, and the first flagellin anchors beneath the distal end of the flagellum to provide a pulling force. Therefore, constant force contributes to a constant growth rate. According to the injection-diffusion model, the secretion system applies a secretion force on an unfolded flagellin, and flagellins are delivered through diffusion after entering the channel. Hence, flagellins are crowded on the channel when the flagellum is getting longer. (B) The chain model predicts a constant growth rate, and the injection-diffusion model predicts a length-dependent growth rate. (C) The summary of flagellar growth rate of three bacteria using fluorescent-based techniques.

Figure 5

A model summarizing the disassembly process of a V. alginolyticus flagellum, showing that it begins with breaking the rod above the MS ring before FliG depolymerization. The C ring, with inner membrane components, then mobilizes on the cell membrane. Finally, the LP ring is likely sealed and the flagellum is ejected.