Biomolecules

Editorial

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3 pages, 180 KiB

Open AccessEditorial

Recent Advances in the Bacterial Flagellar Motor Study

by Tohru Minamino and Keiichi Namba

Biomolecules 2021, 11(5), 741; https://doi.org/10.3390/biom11050741 - 17 May 2021

Viewed by 2866

Abstract

The bacterial flagellum is a supramolecular motility machine that allows bacterial cells to swim in liquid environments [...] Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

Research

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20 pages, 4278 KiB

Open AccessArticle

Fluctuations in Intracellular CheY-P Concentration Coordinate Reversals of Flagellar Motors in E. coli

by Yong-Suk Che, Takashi Sagawa, Yuichi Inoue, Hiroto Takahashi, Tatsuki Hamamoto, Akihiko Ishijima and Hajime Fukuoka

Biomolecules 2020, 10(11), 1544; https://doi.org/10.3390/biom10111544 - 12 Nov 2020

Cited by 10 | Viewed by 3203

Abstract

Signal transduction utilizing membrane-spanning receptors and cytoplasmic regulator proteins is a fundamental process for all living organisms, but quantitative studies of the behavior of signaling proteins, such as their diffusion within a cell, are limited. In this study, we show that fluctuations in [...] Read more.

Signal transduction utilizing membrane-spanning receptors and cytoplasmic regulator proteins is a fundamental process for all living organisms, but quantitative studies of the behavior of signaling proteins, such as their diffusion within a cell, are limited. In this study, we show that fluctuations in the concentration of the signaling molecule, phosphorylated CheY, constitute the basis of chemotaxis signaling. To analyze the propagation of the CheY-P signal quantitatively, we measured the coordination of directional switching between flagellar motors on the same cell. We analyzed the time lags of the switching of two motors in both CCW-to-CW and CW-to-CCW switching (∆τ_CCW-CW and ∆τ_CW-CCW). In wild-type cells, both time lags increased as a function of the relative distance of two motors from the polar receptor array. The apparent diffusion coefficient estimated for ∆τ values was ~9 µm²/s. The distance-dependency of ∆τ_CW-CCW disappeared upon loss of polar localization of the CheY-P phosphatase, CheZ. The distance-dependency of the response time for an instantaneously applied serine attractant signal also disappeared with the loss of polar localization of CheZ. These results were modeled by calculating the diffusion of CheY and CheY-P in cells in which phosphorylation and dephosphorylation occur in different subcellular regions. We conclude that diffusion of signaling molecules and their production and destruction through spontaneous activity of the receptor array generates fluctuations in CheY-P concentration over timescales of several hundred milliseconds. Signal fluctuation coordinates rotation among flagella and regulates steady-state run-and-tumble swimming of cells to facilitate efficient responses to environmental chemical signals. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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11 pages, 1716 KiB

Open AccessArticle

GFP Fusion to the N-Terminus of MotB Affects the Proton Channel Activity of the Bacterial Flagellar Motor in Salmonella

by Yusuke V. Morimoto, Keiichi Namba and Tohru Minamino

Biomolecules 2020, 10(9), 1255; https://doi.org/10.3390/biom10091255 - 29 Aug 2020

Cited by 4 | Viewed by 3334

Abstract

The bacterial flagellar motor converts the energy of proton flow through the MotA/MotB complex into mechanical works required for motor rotation. The rotational force is generated by electrostatic interactions between the stator protein MotA and the rotor protein FliG. The Arg-90 and Glu-98 [...] Read more.

The bacterial flagellar motor converts the energy of proton flow through the MotA/MotB complex into mechanical works required for motor rotation. The rotational force is generated by electrostatic interactions between the stator protein MotA and the rotor protein FliG. The Arg-90 and Glu-98 from MotA interact with Asp-289 and Arg-281 of FliG, respectively. An increase in the expression level of the wild-type MotA/MotB complex inhibits motility of the gfp-motBfliG(R281V) mutant but not the fliG(R281V) mutant, suggesting that the MotA/GFP-MotB complex cannot work together with wild-type MotA/MotB in the presence of the fliG(R281V) mutation. However, it remains unknown why. Here, we investigated the effect of the GFP fusion to MotB at its N-terminus on the MotA/MotB function. Over-expression of wild-type MotA/MotB significantly reduced the growth rate of the gfp-motBfliG(R281V) mutant. The over-expression of the MotA/GFP-MotB complex caused an excessive proton leakage through its proton channel, thereby inhibiting cell growth. These results suggest that the GFP tag on the MotB N-terminus affects well-regulated proton translocation through the MotA/MotB proton channel. Therefore, we propose that the N-terminal cytoplasmic tail of MotB couples the gating of the proton channel with the MotA–FliG interaction responsible for torque generation. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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9 pages, 911 KiB

Open AccessArticle

Coupling Ion Specificity of the Flagellar Stator Proteins MotA1/MotB1 of Paenibacillus sp. TCA20

by Sakura Onoe, Myu Yoshida, Naoya Terahara and Yoshiyuki Sowa

Biomolecules 2020, 10(7), 1078; https://doi.org/10.3390/biom10071078 - 20 Jul 2020

Cited by 4 | Viewed by 2874

Abstract

The bacterial flagellar motor is a reversible rotary molecular nanomachine, which couples ion flux across the cytoplasmic membrane to torque generation. It comprises a rotor and multiple stator complexes, and each stator complex functions as an ion channel and determines the ion specificity [...] Read more.

The bacterial flagellar motor is a reversible rotary molecular nanomachine, which couples ion flux across the cytoplasmic membrane to torque generation. It comprises a rotor and multiple stator complexes, and each stator complex functions as an ion channel and determines the ion specificity of the motor. Although coupling ions for the motor rotation were presumed to be only monovalent cations, such as H⁺ and Na⁺, the stator complex MotA1/MotB1 of Paenibacillus sp. TCA20 (MotA1^TCA/MotB1^TCA) was reported to use divalent cations as coupling ions, such as Ca²⁺ and Mg²⁺. In this study, we initially aimed to measure the motor torque generated by MotA1^TCA/MotB1^TCA under the control of divalent cation motive force; however, we identified that the coupling ion of MotA1^TCAMotB1^TCA is very likely to be a monovalent ion. We engineered a series of functional chimeric stator proteins between MotB1^TCA and Escherichia coli MotB. E. coli ΔmotAB cells expressing MotA1^TCA and the chimeric MotB presented significant motility in the absence of divalent cations. Moreover, we confirmed that MotA1^TCA/MotB1^TCA in Bacillus subtilis ΔmotABΔmotPS cells generates torque without divalent cations. Based on two independent experimental results, we conclude that the MotA1^TCA/MotB1^TCA complex directly converts the energy released from monovalent cation flux to motor rotation. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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14 pages, 2204 KiB

Open AccessArticle

A Novel Lysophosphatidic Acid Acyltransferase of Escherichia coli Produces Membrane Phospholipids with a cis-vaccenoyl Group and Is Related to Flagellar Formation

by Yosuke Toyotake, Masayoshi Nishiyama, Fumiaki Yokoyama, Takuya Ogawa, Jun Kawamoto and Tatsuo Kurihara

Biomolecules 2020, 10(5), 745; https://doi.org/10.3390/biom10050745 - 11 May 2020

Cited by 5 | Viewed by 3512

Abstract

Lysophosphatidic acid acyltransferase (LPAAT) introduces fatty acyl groups into the sn-2 position of membrane phospholipids (PLs). Various bacteria produce multiple LPAATs, whereas it is believed that Escherichia coli produces only one essential LPAAT homolog, PlsC—the deletion of which is lethal. However, we [...] Read more.

Lysophosphatidic acid acyltransferase (LPAAT) introduces fatty acyl groups into the sn-2 position of membrane phospholipids (PLs). Various bacteria produce multiple LPAATs, whereas it is believed that Escherichia coli produces only one essential LPAAT homolog, PlsC—the deletion of which is lethal. However, we found that E. coli possesses another LPAAT homolog named YihG. Here, we show that overexpression of YihG in E. coli carrying a temperature-sensitive mutation in plsC allowed its growth at non-permissive temperatures. Analysis of the fatty acyl composition of PLs from the yihG-deletion mutant (∆yihG) revealed that endogenous YihG introduces the cis-vaccenoyl group into the sn-2 position of PLs. Loss of YihG did not affect cell growth or morphology, but ∆yihG cells swam well in liquid medium in contrast to wild-type cells. Immunoblot analysis showed that FliC was highly expressed in ∆yihG cells, and this phenotype was suppressed by expression of recombinant YihG in ∆yihG cells. Transmission electron microscopy confirmed that the flagellar structure was observed only in ∆yihG cells. These results suggest that YihG has specific functions related to flagellar formation through modulation of the fatty acyl composition of membrane PLs. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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10 pages, 1166 KiB

Open AccessArticle

The Homologous Components of Flagellar Type III Protein Apparatus Have Acquired a Novel Function to Control Twitching Motility in a Non-Flagellated Biocontrol Bacterium

by Alex M. Fulano, Danyu Shen, Miki Kinoshita, Shan-Ho Chou and Guoliang Qian

Biomolecules 2020, 10(5), 733; https://doi.org/10.3390/biom10050733 - 7 May 2020

Cited by 13 | Viewed by 3213

Abstract

The bacterial flagellum is one of the best-studied surface-attached appendages in bacteria. Flagellar assembly in vivo is promoted by its own protein export apparatus, a type III secretion system (T3SS) in pathogenic bacteria. Lysobacter enzymogenes OH11 is a non-flagellated soil bacterium that utilizes [...] Read more.

The bacterial flagellum is one of the best-studied surface-attached appendages in bacteria. Flagellar assembly in vivo is promoted by its own protein export apparatus, a type III secretion system (T3SS) in pathogenic bacteria. Lysobacter enzymogenes OH11 is a non-flagellated soil bacterium that utilizes type IV pilus (T4P)-driven twitching motility to prey upon nearby fungi for food. Interestingly, the strain OH11 encodes components homologous to the flagellar type III protein apparatus (FT3SS) on its genome, but it remains unknown whether this FT3SS-like system is functional. Here, we report that, despite the absence of flagella, the FT3SS homologous genes are responsible not only for the export of the heterologous flagellin in strain OH11 but also for twitching motility. Blocking the FT3SS-like system by in-frame deletion mutations in either flhB or fliI abolished the secretion of heterologous flagellin molecules into the culture medium, indicating that the FT3SS is functional in strain OH11. A deletion of flhA, flhB, fliI, or fliR inhibited T4P-driven twitching motility, whereas neither that of fliP nor fliQ did, suggesting that FlhA, FlhB, FliI, and FliR may obtain a novel function to modulate the twitching motility. The flagellar FliI ATPase was required for the secretion of the major pilus subunit, PilA, suggesting that FliI would have evolved to act as a PilB-like pilus ATPase. These observations lead to a plausible hypothesis that the non-flagellated L. enzymogenes OH11 could preserve FT3SS-like genes for acquiring a distinct function to regulate twitching motility associated with its predatory behavior. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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21 pages, 6067 KiB

Open AccessFeature PaperArticle

MotP Subunit is Critical for Ion Selectivity and Evolution of a K⁺-Coupled Flagellar Motor

by Shun Naganawa and Masahiro Ito

Biomolecules 2020, 10(5), 691; https://doi.org/10.3390/biom10050691 - 29 Apr 2020

Cited by 7 | Viewed by 3535

Abstract

The bacterial flagellar motor is a sophisticated nanomachine embedded in the cell envelope. The flagellar motor is driven by an electrochemical gradient of cations such as H⁺, Na⁺, and K⁺ through ion channels in stator complexes embedded in [...] Read more.

The bacterial flagellar motor is a sophisticated nanomachine embedded in the cell envelope. The flagellar motor is driven by an electrochemical gradient of cations such as H⁺, Na⁺, and K⁺ through ion channels in stator complexes embedded in the cell membrane. The flagellum is believed to rotate as a result of electrostatic interaction forces between the stator and the rotor. In bacteria of the genus Bacillus and related species, the single transmembrane segment of MotB-type subunit protein (MotB and MotS) is critical for the selection of the H⁺ and Na⁺ coupling ions. Here, we constructed and characterized several hybrid stators combined with single Na⁺-coupled and dual Na⁺- and K⁺-coupled stator subunits, and we report that the MotP subunit is critical for the selection of K⁺. This result suggested that the K⁺ selectivity of the MotP/MotS complexes evolved from the single Na⁺-coupled stator MotP/MotS complexes. This finding will promote the understanding of the evolution of flagellar motors and the molecular mechanisms of coupling ion selectivity. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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17 pages, 3130 KiB

Open AccessArticle

A Factor Produced by Kaistia sp. 32K Accelerated the Motility of Methylobacterium sp. ME121

by Yoshiaki Usui, Yuu Wakabayashi, Tetsu Shimizu, Yuhei O. Tahara, Makoto Miyata, Akira Nakamura and Masahiro Ito

Biomolecules 2020, 10(4), 618; https://doi.org/10.3390/biom10040618 - 16 Apr 2020

Cited by 4 | Viewed by 4099

Abstract

Motile Methylobacterium sp. ME121 and non-motile Kaistia sp. 32K were isolated from the same soil sample. Interestingly, ME121 was significantly more motile in the coculture of ME121 and 32K than in the monoculture of ME121. This advanced motility of ME121 was also observed [...] Read more.

Motile Methylobacterium sp. ME121 and non-motile Kaistia sp. 32K were isolated from the same soil sample. Interestingly, ME121 was significantly more motile in the coculture of ME121 and 32K than in the monoculture of ME121. This advanced motility of ME121 was also observed in the 32K culture supernatant. A swimming acceleration factor, which we named the K factor, was identified in the 32K culture supernatant, purified, characterized as an extracellular polysaccharide (5–10 kDa), and precipitated with 70% ethanol. These results suggest the possibility that the K factor was directly or indirectly sensed by the flagellar stator, accelerating the flagellar rotation of ME121. To the best of our knowledge, no reports describing an acceleration in motility due to coculture with two or more types of bacteria have been published. We propose a mechanism by which the increase in rotational force of the ME121 flagellar motor is caused by the introduction of the additional stator into the motor by the K factor. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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11 pages, 2152 KiB

Open AccessFeature PaperArticle

Structural and Functional Comparison of Salmonella Flagellar Filaments Composed of FljB and FliC

by Tomoko Yamaguchi, Shoko Toma, Naoya Terahara, Tomoko Miyata, Masamichi Ashihara, Tohru Minamino, Keiichi Namba and Takayuki Kato

Biomolecules 2020, 10(2), 246; https://doi.org/10.3390/biom10020246 - 6 Feb 2020

Cited by 37 | Viewed by 7012

Abstract

The bacterial flagellum is a motility organelle consisting of a long helical filament as a propeller and a rotary motor that drives rapid filament rotation to produce thrust. Salmonella enterica serovar Typhimurium has two genes of flagellin, fljB and fliC, for flagellar [...] Read more.

The bacterial flagellum is a motility organelle consisting of a long helical filament as a propeller and a rotary motor that drives rapid filament rotation to produce thrust. Salmonella enterica serovar Typhimurium has two genes of flagellin, fljB and fliC, for flagellar filament formation and autonomously switches their expression at a frequency of 10⁻³–10⁻⁴ per cell per generation. We report here differences in their structures and motility functions under high-viscosity conditions. A Salmonella strain expressing FljB showed a higher motility than one expressing FliC under high viscosity. To examine the reasons for this motility difference, we carried out structural analyses of the FljB filament by electron cryomicroscopy and found that the structure was nearly identical to that of the FliC filament except for the position and orientation of the outermost domain D3 of flagellin. The density of domain D3 was much lower in FljB than FliC, suggesting that domain D3 of FljB is more flexible and mobile than that of FliC. These differences suggest that domain D3 plays an important role not only in changing antigenicity of the filament but also in optimizing motility function of the filament as a propeller under different conditions. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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14 pages, 2391 KiB

Open AccessArticle

In Vitro Autonomous Construction of the Flagellar Axial Structure in Inverted Membrane Vesicles

by Hiroyuki Terashima, Chinatsu Tatsumi, Akihiro Kawamoto, Keiichi Namba, Tohru Minamino and Katsumi Imada

Biomolecules 2020, 10(1), 126; https://doi.org/10.3390/biom10010126 - 11 Jan 2020

Cited by 8 | Viewed by 4962

Abstract

The bacterial flagellum is a filamentous organelle extending from the cell surface. The axial structure of the flagellum consists of the rod, hook, junction, filament, and cap. The axial structure is formed by axial component proteins exported via a specific protein export apparatus [...] Read more.

The bacterial flagellum is a filamentous organelle extending from the cell surface. The axial structure of the flagellum consists of the rod, hook, junction, filament, and cap. The axial structure is formed by axial component proteins exported via a specific protein export apparatus in a well-regulated manner. Although previous studies have revealed the outline of the flagellar construction process, the mechanism of axial structure formation, including axial protein export, is still obscure due to difficulties in direct observation of protein export and assembly in vivo. We recently developed an in vitro flagellar protein transport assay system using inverted membrane vesicles (IMVs) and succeeded in reproducing the early stage of flagellar assembly. However, the late stage of the flagellar formation process remained to be examined in the IMVs. In this study, we showed that the filament-type proteins are transported into the IMVs to produce the filament on the hook inside the IMVs. Furthermore, we provide direct evidence that coordinated flagellar protein export and assembly can occur at the post-translational level. These results indicate that the ordered construction of the entire flagellar structure can be regulated by only the interactions between the protein export apparatus, the export substrate proteins, and their cognate chaperones. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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13 pages, 5308 KiB

Open AccessFeature PaperArticle

Structure of Salmonella Flagellar Hook Reveals Intermolecular Domain Interactions for the Universal Joint Function

by Péter Horváth, Takayuki Kato, Tomoko Miyata and Keiichi Namba

Biomolecules 2019, 9(9), 462; https://doi.org/10.3390/biom9090462 - 9 Sep 2019

Cited by 19 | Viewed by 4040

Abstract

The bacterial flagellum is a motility organelle consisting of a rotary motor and a long helical filament as a propeller. The flagellar hook is a flexible universal joint that transmits motor torque to the filament in its various orientations that change dynamically between [...] Read more.

The bacterial flagellum is a motility organelle consisting of a rotary motor and a long helical filament as a propeller. The flagellar hook is a flexible universal joint that transmits motor torque to the filament in its various orientations that change dynamically between swimming and tumbling of the cell upon switching the motor rotation for chemotaxis. Although the structures of the hook and hook protein FlgE from different bacterial species have been studied, the structure of Salmonella hook, which has been studied most over the years, has not been solved at a high enough resolution to allow building an atomic model of entire FlgE for understanding the mechanisms of self-assembly, stability and the universal joint function. Here we report the structure of Salmonella polyhook at 4.1 Å resolution by electron cryomicroscopy and helical image analysis. The density map clearly revealed folding of the entire FlgE chain forming the three domains D0, D1 and D2 and allowed us to build an atomic model. The model includes domain Dc with a long β-hairpin structure that connects domains D0 and D1 and contributes to the structural stability of the hook while allowing the flexible bending of the hook as a molecular universal joint. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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11 pages, 3108 KiB

Open AccessArticle

Architecture of the Bacterial Flagellar Distal Rod and Hook of Salmonella

by Yumiko Saijo-Hamano, Hideyuki Matsunami, Keiichi Namba and Katsumi Imada

Biomolecules 2019, 9(7), 260; https://doi.org/10.3390/biom9070260 - 7 Jul 2019

Cited by 14 | Viewed by 4903

Abstract

The bacterial flagellum is a large molecular complex composed of thousands of protein subunits for motility. The filamentous part of the flagellum, which is called the axial structure, consists of the filament, the hook, and the rods, with other minor components—the cap protein [...] Read more.

The bacterial flagellum is a large molecular complex composed of thousands of protein subunits for motility. The filamentous part of the flagellum, which is called the axial structure, consists of the filament, the hook, and the rods, with other minor components—the cap protein and the hook associated proteins. They share a common basic architecture of subunit arrangement, but each part shows quite distinct mechanical properties to achieve its specific function. The distal rod and the hook are helical assemblies of a single protein, FlgG and FlgE, respectively. They show a significant sequence similarity but have distinct mechanical characteristics. The rod is a rigid, straight cylinder, whereas the hook is a curved tube with high bending flexibility. Here, we report a structural model of the rod constructed by using the crystal structure of a core fragment of FlgG with a density map obtained previously by electron cryomicroscopy. Our structural model suggests that a segment called L-stretch plays a key role in achieving the distinct mechanical properties of the rod using a structurally similar component protein to that of the hook. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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Review

Jump to: Editorial, Research

18 pages, 1707 KiB

Open AccessFeature PaperReview

Protein Export via the Type III Secretion System of the Bacterial Flagellum

by Manuel Halte and Marc Erhardt

Biomolecules 2021, 11(2), 186; https://doi.org/10.3390/biom11020186 - 29 Jan 2021

Cited by 23 | Viewed by 5045

Abstract

The bacterial flagellum and the related virulence-associated injectisome system of pathogenic bacteria utilize a type III secretion system (T3SS) to export substrate proteins across the inner membrane in a proton motive force-dependent manner. The T3SS is composed of an export gate (FliPQR/FlhA/FlhB) located [...] Read more.

The bacterial flagellum and the related virulence-associated injectisome system of pathogenic bacteria utilize a type III secretion system (T3SS) to export substrate proteins across the inner membrane in a proton motive force-dependent manner. The T3SS is composed of an export gate (FliPQR/FlhA/FlhB) located in the flagellar basal body and an associated soluble ATPase complex in the cytoplasm (FliHIJ). Here, we summarise recent insights into the structure, assembly and protein secretion mechanisms of the T3SS with a focus on energy transduction and protein transport across the cytoplasmic membrane. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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14 pages, 3800 KiB

Open AccessReview

Construction and Loss of Bacterial Flagellar Filaments

by Xiang-Yu Zhuang and Chien-Jung Lo

Biomolecules 2020, 10(11), 1528; https://doi.org/10.3390/biom10111528 - 9 Nov 2020

Cited by 14 | Viewed by 4991

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 [...] Read more.

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. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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24 pages, 1511 KiB

Open AccessFeature PaperEditor’s ChoiceReview

Structural Conservation and Adaptation of the Bacterial Flagella Motor

by Brittany L. Carroll and Jun Liu

Biomolecules 2020, 10(11), 1492; https://doi.org/10.3390/biom10111492 - 29 Oct 2020

Cited by 27 | Viewed by 10921

Abstract

Many bacteria require flagella for the ability to move, survive, and cause infection. The flagellum is a complex nanomachine that has evolved to increase the fitness of each bacterium to diverse environments. Over several decades, molecular, biochemical, and structural insights into the flagella [...] Read more.

Many bacteria require flagella for the ability to move, survive, and cause infection. The flagellum is a complex nanomachine that has evolved to increase the fitness of each bacterium to diverse environments. Over several decades, molecular, biochemical, and structural insights into the flagella have led to a comprehensive understanding of the structure and function of this fascinating nanomachine. Notably, X-ray crystallography, cryo-electron microscopy (cryo-EM), and cryo-electron tomography (cryo-ET) have elucidated the flagella and their components to unprecedented resolution, gleaning insights into their structural conservation and adaptation. In this review, we focus on recent structural studies that have led to a mechanistic understanding of flagellar assembly, function, and evolution. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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26 pages, 5642 KiB

Open AccessReview

The Architectural Dynamics of the Bacterial Flagellar Motor Switch

by Shahid Khan

Biomolecules 2020, 10(6), 833; https://doi.org/10.3390/biom10060833 - 29 May 2020

Cited by 7 | Viewed by 3680

Abstract

The rotary bacterial flagellar motor is remarkable in biochemistry for its highly synchronized operation and amplification during switching of rotation sense. The motor is part of the flagellar basal body, a complex multi-protein assembly. Sensory and energy transduction depends on a core of [...] Read more.

The rotary bacterial flagellar motor is remarkable in biochemistry for its highly synchronized operation and amplification during switching of rotation sense. The motor is part of the flagellar basal body, a complex multi-protein assembly. Sensory and energy transduction depends on a core of six proteins that are adapted in different species to adjust torque and produce diverse switches. Motor response to chemotactic and environmental stimuli is driven by interactions of the core with small signal proteins. The initial protein interactions are propagated across a multi-subunit cytoplasmic ring to switch torque. Torque reversal triggers structural transitions in the flagellar filament to change motile behavior. Subtle variations in the core components invert or block switch operation. The mechanics of the flagellar switch have been studied with multiple approaches, from protein dynamics to single molecule and cell biophysics. The architecture, driven by recent advances in electron cryo-microscopy, is available for several species. Computational methods have correlated structure with genetic and biochemical databases. The design principles underlying the basis of switch ultra-sensitivity and its dependence on motor torque remain elusive, but tantalizing clues have emerged. This review aims to consolidate recent knowledge into a unified platform that can inspire new research strategies. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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14 pages, 2515 KiB

Open AccessReview

Living in a Foster Home: The Single Subpolar Flagellum Fla1 of Rhodobacter sphaeroides

by Laura Camarena and Georges Dreyfus

Biomolecules 2020, 10(5), 774; https://doi.org/10.3390/biom10050774 - 16 May 2020

Cited by 6 | Viewed by 4099

Abstract

Rhodobacter sphaeroides is an α-proteobacterium that has the particularity of having two functional flagellar systems used for swimming. Under the growth conditions commonly used in the laboratory, a single subpolar flagellum that traverses the cell membrane, is assembled on the surface. This flagellum [...] Read more.

Rhodobacter sphaeroides is an α-proteobacterium that has the particularity of having two functional flagellar systems used for swimming. Under the growth conditions commonly used in the laboratory, a single subpolar flagellum that traverses the cell membrane, is assembled on the surface. This flagellum has been named Fla1. Phylogenetic analyses have suggested that this flagellar genetic system was acquired from an ancient γ-proteobacterium. It has been shown that this flagellum has components homologous to those present in other γ-proteobacteria such as the H-ring characteristic of the Vibrio species. Other features of this flagellum such as a straight hook, and a prominent HAP region have been studied and the molecular basis underlying these features has been revealed. It has also been shown that FliL, and the protein MotF, mainly found in several species of the family Rhodobacteraceae, contribute to remodel the amphipathic region of MotB, known as the plug, in order to allow flagellar rotation. In the absence of the plug region of MotB, FliL and MotF are dispensable. In this review we have covered the most relevant aspects of the Fla1 flagellum of this remarkable photosynthetic bacterium. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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16 pages, 2327 KiB

Open AccessReview

Spirochete Flagella and Motility

by Shuichi Nakamura

Biomolecules 2020, 10(4), 550; https://doi.org/10.3390/biom10040550 - 4 Apr 2020

Cited by 35 | Viewed by 13110

Abstract

Spirochetes can be distinguished from other flagellated bacteria by their long, thin, spiral (or wavy) cell bodies and endoflagella that reside within the periplasmic space, designated as periplasmic flagella (PFs). Some members of the spirochetes are pathogenic, including the causative agents of syphilis, [...] Read more.

Spirochetes can be distinguished from other flagellated bacteria by their long, thin, spiral (or wavy) cell bodies and endoflagella that reside within the periplasmic space, designated as periplasmic flagella (PFs). Some members of the spirochetes are pathogenic, including the causative agents of syphilis, Lyme disease, swine dysentery, and leptospirosis. Furthermore, their unique morphologies have attracted attention of structural biologists; however, the underlying physics of viscoelasticity-dependent spirochetal motility is a longstanding mystery. Elucidating the molecular basis of spirochetal invasion and interaction with hosts, resulting in the appearance of symptoms or the generation of asymptomatic reservoirs, will lead to a deeper understanding of host–pathogen relationships and the development of antimicrobials. Moreover, the mechanism of propulsion in fluids or on surfaces by the rotation of PFs within the narrow periplasmic space could be a designing base for an autonomously driving micro-robot with high efficiency. This review describes diverse morphology and motility observed among the spirochetes and further summarizes the current knowledge on their mechanisms and relations to pathogenicity, mainly from the standpoint of experimental biophysics. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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17 pages, 4598 KiB

Open AccessFeature PaperReview

Regulation of the Single Polar Flagellar Biogenesis

by Seiji Kojima, Hiroyuki Terashima and Michio Homma

Biomolecules 2020, 10(4), 533; https://doi.org/10.3390/biom10040533 - 1 Apr 2020

Cited by 18 | Viewed by 5277

Abstract

Some bacterial species, such as the marine bacterium Vibrio alginolyticus, have a single polar flagellum that allows it to swim in liquid environments. Two regulators, FlhF and FlhG, function antagonistically to generate only one flagellum at the cell pole. FlhF, a signal recognition [...] Read more.

Some bacterial species, such as the marine bacterium Vibrio alginolyticus, have a single polar flagellum that allows it to swim in liquid environments. Two regulators, FlhF and FlhG, function antagonistically to generate only one flagellum at the cell pole. FlhF, a signal recognition particle (SRP)-type guanosine triphosphate (GTP)ase, works as a positive regulator for flagellar biogenesis and determines the location of flagellar assembly at the pole, whereas FlhG, a MinD-type ATPase, works as a negative regulator that inhibits flagellar formation. FlhF intrinsically localizes at the cell pole, and guanosine triphosphate (GTP) binding to FlhF is critical for its polar localization and flagellation. FlhG also localizes at the cell pole via the polar landmark protein HubP to directly inhibit FlhF function at the cell pole, and this localization depends on ATP binding to FlhG. However, the detailed regulatory mechanisms involved, played by FlhF and FlhG as the major factors, remain largely unknown. This article reviews recent studies that highlight the post-translational regulation mechanism that allows the synthesis of only a single flagellum at the cell pole. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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14 pages, 1068 KiB

Open AccessReview

Flagella and Swimming Behavior of Marine Magnetotactic Bacteria

by Wei-Jia Zhang and Long-Fei Wu

Biomolecules 2020, 10(3), 460; https://doi.org/10.3390/biom10030460 - 16 Mar 2020

Cited by 18 | Viewed by 5498

Abstract

Marine environments are generally characterized by low bulk concentrations of nutrients that are susceptible to steady or intermittent motion driven by currents and local turbulence. Marine bacteria have therefore developed strategies, such as very fast-swimming and the exploitation of multiple directional sensing–response systems [...] Read more.

Marine environments are generally characterized by low bulk concentrations of nutrients that are susceptible to steady or intermittent motion driven by currents and local turbulence. Marine bacteria have therefore developed strategies, such as very fast-swimming and the exploitation of multiple directional sensing–response systems in order to efficiently migrate towards favorable places in nutrient gradients. The magnetotactic bacteria (MTB) even utilize Earth’s magnetic field to facilitate downward swimming into the oxic–anoxic interface, which is the most favorable place for their persistence and proliferation, in chemically stratified sediments or water columns. To ensure the desired flagella-propelled motility, marine MTBs have evolved an exquisite flagellar apparatus, and an extremely high number (tens of thousands) of flagella can be found on a single entity, displaying a complex polar, axial, bounce, and photosensitive magnetotactic behavior. In this review, we describe gene clusters, the flagellar apparatus architecture, and the swimming behavior of marine unicellular and multicellular magnetotactic bacteria. The physiological significance and mechanisms that govern these motions are discussed. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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15 pages, 1562 KiB

Open AccessReview

Phylogenetic Distribution, Ultrastructure, and Function of Bacterial Flagellar Sheaths

by Joshua Chu, Jun Liu and Timothy R. Hoover

Biomolecules 2020, 10(3), 363; https://doi.org/10.3390/biom10030363 - 27 Feb 2020

Cited by 26 | Viewed by 5271

Abstract

A number of Gram-negative bacteria have a membrane surrounding their flagella, referred to as the flagellar sheath, which is continuous with the outer membrane. The flagellar sheath was initially described in Vibrio metschnikovii in the early 1950s as an extension of the outer [...] Read more.

A number of Gram-negative bacteria have a membrane surrounding their flagella, referred to as the flagellar sheath, which is continuous with the outer membrane. The flagellar sheath was initially described in Vibrio metschnikovii in the early 1950s as an extension of the outer cell wall layer that completely surrounded the flagellar filament. Subsequent studies identified other bacteria that possess flagellar sheaths, most of which are restricted to a few genera of the phylum Proteobacteria. Biochemical analysis of the flagellar sheaths from a few bacterial species revealed the presence of lipopolysaccharide, phospholipids, and outer membrane proteins in the sheath. Some proteins localize preferentially to the flagellar sheath, indicating mechanisms exist for protein partitioning to the sheath. Recent cryo-electron tomography studies have yielded high resolution images of the flagellar sheath and other structures closely associated with the sheath, which has generated insights and new hypotheses for how the flagellar sheath is synthesized. Various functions have been proposed for the flagellar sheath, including preventing disassociation of the flagellin subunits in the presence of gastric acid, avoiding activation of the host innate immune response by flagellin, activating the host immune response, adherence to host cells, and protecting the bacterium from bacteriophages. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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23 pages, 2555 KiB

Open AccessEditor’s ChoiceReview

Flagella-Driven Motility of Bacteria

by Shuichi Nakamura and Tohru Minamino

Biomolecules 2019, 9(7), 279; https://doi.org/10.3390/biom9070279 - 14 Jul 2019

Cited by 215 | Viewed by 27202

Abstract

The bacterial flagellum is a helical filamentous organelle responsible for motility. In bacterial species possessing flagella at the cell exterior, the long helical flagellar filament acts as a molecular screw to generate thrust. Meanwhile, the flagella of spirochetes reside within the periplasmic space [...] Read more.

The bacterial flagellum is a helical filamentous organelle responsible for motility. In bacterial species possessing flagella at the cell exterior, the long helical flagellar filament acts as a molecular screw to generate thrust. Meanwhile, the flagella of spirochetes reside within the periplasmic space and not only act as a cytoskeleton to determine the helicity of the cell body, but also rotate or undulate the helical cell body for propulsion. Despite structural diversity of the flagella among bacterial species, flagellated bacteria share a common rotary nanomachine, namely the flagellar motor, which is located at the base of the filament. The flagellar motor is composed of a rotor ring complex and multiple transmembrane stator units and converts the ion flux through an ion channel of each stator unit into the mechanical work required for motor rotation. Intracellular chemotactic signaling pathways regulate the direction of flagella-driven motility in response to changes in the environments, allowing bacteria to migrate towards more desirable environments for their survival. Recent experimental and theoretical studies have been deepening our understanding of the molecular mechanisms of the flagellar motor. In this review article, we describe the current understanding of the structure and dynamics of the bacterial flagellum. Full article

(This article belongs to the Special Issue Perspectives on Bacterial Flagellar Motor)

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