A “Mechanistic” Explanation of the Multiple Helical Forms Adopted by Bacterial Flagellar Filaments

Abstract

The corkscrew-like flagellar filaments emerging from the surface of bacteria such as Salmonella typhimurium propel the cells toward nutrient and away from repellents. This kind of motility depends upon the ability of the flagellar filaments to adopt a range of distinct helical forms. A filament is typically constructed from ~ 30,000 identical flagellin molecules, which self-assemble into a tubular structure containing 11 near-longitudinal protofilaments. A “mechanical” model, in which the flagellin building block has the capacity to switch between two principal interfacial states, predicts that the filament can assemble into a “canonical” family of 12 distinct helical forms, each having unique curvature and twist: these include two “extreme” straight forms having left- and right-handed twists, respectively, and 10 intermediate helical forms. Measured shapes of the filaments correspond well with predictions of the model. This report is concerned with two unanswered questions. First, what properties of the flagellin determine which of the 12 discrete forms is preferred? Second, how does the interfacial “switch” work, at a molecular level? Our proposed solution of these problems is based mainly on a detailed examination of differences between the available electron cryo-microscopy structures of the straight L and R filaments, respectively.

Multiple Flagellin Proteins Have Distinct and Synergistic Roles in Agrobacterium tumefaciens Motility

“…Transitions between these polymorphisms under hydrodynamic torque as a result of flagellar motor rotation reversal are responsible for flagellar bundle disruption, leading to tumbles in peritrichous multiflagellated bacteria. Each flagellin monomer can exist in one of two conformational states, L-type and R-type (that differ slightly in length), leading to L-or R-type protofilaments, given the high degree of cooperativity among subunits along each protofilament (39)(40)(41). When all protofilaments are L or R type, the flagellum is straight, while different proportions correspond to different ratios of L-and R-type monomers (38).…”

Physics of microswimmers—single particle motion and collective behavior: a review

“…which implies a random reorientation of the bacterium (stage 3 and 4). The reversal of the rotational direction is accompanied by a change of the helical handedness from left-handed to right-handed and the flagellum undergoes a polymorphic transition (Armitage and Macnab, 1987;Calladine, 1975;Calladine et al, 2013;Macnab, 1977;Shah et al, 2000;Stark, 2010, 2013). At the end of the "tumbling" phase, all flagella start to rotate again in the same counterclockwise direction (stage 5), the bundle reforms (stage 6), and the bacterium returns to a directional motion (stage 7 and 8).…”

Transcriptional Control of the Lateral-Flagellar Genes of Bradyrhizobium diazoefficiens

“…For the second task, the basal body contains the flagellar motor, composed of a stator in the inner cell membrane and a rotor formed by a ring of several protein subunits that rotates inside the stator by the proton or sodium ion motive force. In turn, the hook and the filament are formed by the polymerization of thousands of monomers of structural proteins and are held together by specific hook-filament junctions (7,8). The hook is a flexible connector that transmits motor rotation in the form of waves to the flagellar filament, whose extension in turn rotates while undulating like an Archimedean screw to drag or thrust the cell in an aqueous medium, depending on whether the flagellum is ahead or behind the cell, respectively (9).…”