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Structural Conservation and Adaptation of the Bacterial Flagella Motor biomolecules Review Structural Conservation and Adaptation of the Bacterial Flagella Motor Brittany L. Carroll 1,2 and Jun Liu 1,2,* 1 Department of Microbial Pathogenesis, Yale School of Medicine, New Haven, CT 06536, USA; [email protected] 2 Microbial Sciences Institute, Yale University, West Haven, CT 06516, USA * Correspondence: [email protected] Received: 5 October 2020; Accepted: 27 October 2020; Published: 29 October 2020 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 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. Keywords: bacterial flagellum; cryo-electron tomography; cryo-electron microscopy; molecular motor; structure and function; torque generation; evolution 1. Introduction The flagellum, a complex nanomachine, propels bacteria through media and along surfaces, using an ion gradient across the cytoplasmic membrane (for review [1]). All flagella share basic structural elements, including the filament, hook, and motor (Figure1A). The filament acts as the propeller guiding the bacterium through space, while the hook acts as a joint transmitting energy from the motor to the filament [2–6]. The motor, or basal body is homologous to the non-flagellar type III secretion system (T3SS) (for review [7]). The filament can present either externally (Figure1B,C) or periplasmically (Figure1D). External flagella extend through the outer membrane into the media surrounding the bacterium and can further be categorized as lateral, peritrichous, and polar [8], while periplasmic flagella reside within the periplasmic space and are essential for spirochete motility [9]. The flagella of Salmonella enterica (henceforth called Salmonella) and Escherichia coli possess the best-studied motors, consisting of the membrane/supramembrane (MS) ring, cytoplasmic (C) ring, peptidoglycan (P) ring, lipopolysaccharide (L) ring, rod, stator, and export apparatus. The MS ring (FliF) acts a base upon which the motor sits, and the C ring (FliG, FliM, and FliN) controls the rotation sense [10–16]. The stator generates torque through ion gradients, mainly H+ (MotA and MotB) and sometimes Na+ (PomA and PomB), which drives the rotation of the C ring [14,15,17–19]. The rod (FlgB, FlgC, and FlgF, and FlgG) acts as a drive shaft, connecting the MS ring to the hook [20–22], and the L (FlgH) and P (FlgI) rings act as the bushings, providing support to the rotating rod [23]. The export gate complex, (FlhA, FlhB, FliP, FliQ, and FliR) and ATPase complex (FliH, FliI, and FliJ) [24–26] are responsible for the temporal and spatial assembly, ensuring that a functional flagellum is built [27]. Advances in structural biology techniques, specifically cryo-electron microscopy (cryo-EM) and cryo-electron tomography (cryo-ET), have led to the investigation of flagella from many Biomolecules 2020, 10, 1492; doi:10.3390/biom10111492 www.mdpi.com/journal/biomolecules Biomolecules 2020, 10, 1492 2 of 24 Biomolecules 2020, 10, x 2 of 24 othercryo-electron species, resulting tomography in the (cryo-ET), identification have led of to conserved the investigation and specifically of flagella from adapted many structural other species, features. Cryo-ETresulting uniquely in the allows identification for the of visualization conserved and of flagellarspecifically structures adapted instructural situ, without features. the Cryo-ET necessity of isolationuniquely and allows purification for the ofvisualization the complexes. of flagellar In this structures review, in we situ summarize, without the the necessity plethora of isolation of structural workand that purification has widened of the our complexes. view of theIn this assembly, review, adaptation,we summarize and the evolution plethora of of structural bacterial work flagella. that has widened our view of the assembly, adaptation, and evolution of bacterial flagella. FigureFigure 1. Bacterial 1. Bacterial flagella flagella control control distinct distinct motility.motility. The The flagellar flagellar motor motor is a is complex a complex nanomachine nanomachine that drives filament rotation. (A) Cartoon model of the flagellar motor. (B) In the two-step model used that drives filament rotation. (A) Cartoon model of the flagellar motor. (B) In the two-step model by many species, such as E. coli and Salmonella, the cell body is propelled forward, or runs, during used by many species, such as E. coli and Salmonella, the cell body is propelled forward, or runs, counterclockwise (looking from the motor to the filament, CCW) rotation, and the filaments form an duringorganized counterclockwise bundle. To change (looking direction, from the the motor cell tumble to thes filament,by rotating CCW) the filament rotation, in the and clockwise the filaments (CW) form an organizeddirection, bundle.unwinding To the change bundle. direction, (C) Vibriothe spp. cell usetumbles a three-step by method, rotating with the filamentCCW rotation in the moving clockwise (CW)the direction, cell body unwinding forward, CW the rotation bundle. moving (C) Vibriothe cellspp. body usein reverse, a three-step and a flicking method, motion with when CCW CW- rotation movingto-CCW the cellrandomly body change forward, direction. CW rotation (D) Spirochetes, moving with the cellperiplasmic body in flagella reverse, at both and poles, a flicking require motion whena CW-to-CCWunique two-step randomly method. change During direction.the run, the (D flag) Spirochetes,ella rotate CCW with and periplasmic CW at opposite flagella poles, at both such poles, requirethat a one unique pole two-step“pulls” while method. the other During “pushes”. the run, Both the poles flagella rotate rotate in the CCW CW direction and CW while at opposite the cell poles, suchtumbles that one to pole change “pulls” direction. while the other “pushes”. Both poles rotate in the CW direction while the cell tumbles to change direction. 2. The Bacterial Flagellar Structure 2. The BacterialStructural Flagellar studies have Structure illustrated how the flagellum is assembled and the unique features that Structuralhave evolved studies in different have illustrated species. X-ray how crystallography the flagellum isis assembledparticularly and powerful the unique in unveiling features many that have atomic structures of individual flagellar proteins as well as small subcomplexes (Table 1). These evolved in different species. X-ray crystallography is particularly powerful in unveiling many atomic atomic models provide invaluable insight into the individual proteins and protein–protein structures of individual flagellar proteins as well as small subcomplexes (Table1). These atomic models interactions involved in flagellar assembly and aid in designing functional studies. Recently, cryo- provideEM invaluablehas been increasingly insight into utilized the individualto provide both proteins medium- and and protein–protein high-resolution interactions structures of involved many in flagellarflagellar assembly subcomplexes, and aid inelucidating designing variable functional symmetry studies. and Recently, complexity cryo-EM of the hasmotor been (Table increasingly 2). utilizedHowever, to provide the flagellum both medium- as an intact and organelle high-resolution is far too complex structures and flexible of many for X-ray flagellar crystallography subcomplexes, elucidatingand cryo-EM. variable Cryo-ET symmetry coupled and with complexity subtomogram of the averaging motor (Table[28] has2). the However, unique capacity the flagellum to reveal as an intactthe organelle entirety isof far bacterial too complex flagella and in multiple flexible spec for X-rayies, depicting crystallography the relative and arrangement cryo-EM. Cryo-ET of the rings coupled with subtomogram averaging [28] has the unique capacity to reveal the entirety of bacterial flagella in multiple species, depicting the relative arrangement of the rings and other protein complexes of the flagella in situ (Table3). In this section, we review the structural information that not only is conserved but also provides a basis for understanding the functions. Biomolecules 2020, 10, 1492 3 of 24 Table 1. Crystal structures of flagellar proteins. A list of the flagellar protein structures deposited in the PDB. Protein(s) Species PDB ID Refs Axial Bacillus cereus 5Z7Q [29] Salmonella typhimurium 1IO1 [30] Flagellin Sphingaomonas sp 2ZBI, 3K8V, 3K8W [31] FliC Burkholderia psuedomallei 4CFI [32] Pseudomonas aeruginosa 4NX9 [33] Aquifex aeolicus 1ORY, 1ORJ [34] FliS Bacillus cereus 5XEF [35] Helicobacter pylori 3IQC [36] Salmonella typhimurium 5GNA FliT Yersinia enterocolitica 3NKZ FljB Salmonella typhimurium 6RGV [37] FcpA Leptospira biflexa 6NQY [38] FcpB Leptospira interrogans 6NQZ [38] Flagellin–FliS Bacillus subtilis 5MAW, 6GOW [39] FliC–FliS fusion Aquifex aeolicus 4IWB [40] Helicobacter pylori 4ZZF, 4ZZK, 5K5Y [41,42] FlgD Salmonella typhimurium 6IEE, 6IEF Campylobacter jejuni
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