Motility often plays a decisive role in the survival of species. Five systems of motility have been studied in depth: those propelled by bacterial flagella, eukaryotic actin polymerization and the eukaryotic motor proteins myosin, kinesin and dynein. However, many organisms exhibit surprisingly diverse motilities, and advances in genomics, molecular biology and imaging have showed that those motilities have inherently independent mechanisms. This makes defining the breadth of motility nontrivial, because novel motilities may be driven by unknown mechanisms. Here, we classify the known motilities based on the unique classes of movement‐producing protein architectures. Based on this criterion, the current total of independent motility systems stands at 18 types. In this perspective, we discuss these modes of motility relative to the latest phylogenetic Tree of Life and propose a history of motility. During the ~4 billion years since the emergence of life, motility arose in Bacteria with flagella and pili, and in Archaea with archaella. Newer modes of motility became possible in Eukarya with changes to the cell envelope. Presence or absence of a peptidoglycan layer, the acquisition of robust membrane dynamics, the enlargement of cells and environmental opportunities likely provided the context for the (co)evolution of novel types of motility.

Summary: Torque generation in the Salmonella flagellar motor is coupled to translocation of H⁺ ions through the proton‐conducting channel of the Mot protein stator complex. The Mot complex is believed to be anchored to the peptidoglycan (PG) layer by the putative peptidoglycan‐binding (PGB) domain of MotB. Proton translocation is activated only when the stator is installed into the motor. We report the crystal structure of a C‐terminal periplasmic fragment of MotB (MotB_C) that contains the PGB domain and includes the entire periplasmic region essential for motility. Structural and functional analyses indicate that the PGB domains must dimerize in order to form the proton‐conducting channel. Drastic conformational changes in the N‐terminal portion of MotB_C are required both for PG binding and the proton channel activation.

Summary: The bacterial flagellar motor is driven by the electrochemical potential of specific ions, H⁺ or Na⁺. The motor consists of a rotor and stator, and their interaction generates rotation. The stator, which is composed of PomA and PomB in the Na⁺ motor of Vibrio alginolyticus, is thought to be a torque generator converting the energy of ion flux into mechanical power. We found that specific mutations in PomB, including D24N, F33C and S248F, which caused motility defects, affected the assembly of stator complexes into the polar flagellar motor using green fluorescent protein‐fused stator proteins. D24 of PomB is the predicted Na⁺‐binding site. Furthermore, we demonstrated that the coupling ion, Na⁺, is required for stator assembly and that phenamil (an inhibitor of the Na⁺‐driven motor) inhibited the assembly. Carbonyl cyanide m‐chlorophenylhydrazone, which is a proton ionophore that collapses the sodium motive force in this organism at neutral pH, also inhibited the assembly. Thus we conclude that the process of Na⁺ influx through the channel, including Na⁺ binding, is essential for the assembly of the stator complex to the flagellar motor as well as for torque generation.

Vibrio species are Gram-negative, rod-shaped bacteria that live in aqueous environments. Several species, such as V. harveyi, V. alginotyticus and V. splendidus, are associated with diseases in fish or shellfish. In addition, a few species, such as V. cholerae and V. parahaemolyticus, are risky for humans due to infections from eating raw shellfish infected with these bacteria or from exposure of wounds to the marine environment. Bacterial flagella are not essential to live in a culture medium. However, most Vibrio species are motile and have rotating flagella which allow them to move into favorable environments or to escape from unfavorable environments. This review summarizes recent studies about the flagellar structure, function, and regulation of Vibrio species, especially focused on the Na+-driven polar flagella that are principally responsible for motility and sensing the surrounding environment, and discusses the relationship between flagella and pathogenicity.

Significance: Many important bacterial pathogens such as Vibrio cholerae and Helicobacter pylori use a sheathed flagellum as the main organelle for motility. Although bacterial flagella have been extensively studied in model systems such as Escherichia coli and Salmonella , relatively little is known about sheathed flagella. In this study, we use high-throughput cryoelectron tomography to visualize thousands of polar flagella in Vibrio alginolyticus . We not only reveal unprecedented details of sheathed flagella in V. alginolyticus but also uncover key differences between sheathed flagella and unsheathed flagella in the same Vibrio species. Our studies provide insight into the unique aspects of sheathed flagella, which are effectively used by many bacterial pathogens to establish infection and disseminate in humans and other mammalian hosts.

Rotation of the sodium-driven polar flagellum of Vibrio alginolyticus requires four motor proteins: PomA, PomB, MotX, and MotY. PomA and PomB form a sodium-ion channel in the cytoplasmic membrane that functions as a stator complex to couple sodium-ion flux with torque generation. MotX and MotY are components of the T-ring, which is located beneath the P-ring of the polar flagellar basal body and is involved in incorporation of the PomA/PomB complex into the motor. Here, we describe the determination of the crystal structure of MotY at 2.9 Å resolution. The structure shows two distinct domains: an N-terminal domain (MotY-N) and a C-terminal domain (MotY-C). MotY-N has a unique structure. MotY-C contains a putative peptidoglycan-binding motif that is remarkably similar to those of peptidoglycan-binding proteins, such as Pal and RmpM, but this region is disordered in MotY. Motility assay of cells producing either of the MotY-N and MotY-C fragments and subsequent biochemical analyses indicate that MotY-N is essential for association of the stator units around the rotor, whereas MotY-C stabilizes the association by binding to the peptidoglycan layer. Based on these observations, we propose a model for the mechanism of stator assembly around the rotor.