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Spirochete Flagella and Motility biomolecules Review Spirochete Flagella and Motility Shuichi Nakamura Department of Applied Physics, Graduate School of Engineering, Tohoku University, 6-6-05 Aoba, Aoba-ku, Sendai, Miyagi 980-8579, Japan; [email protected]; Tel.: +81-22-795-5849 Received: 11 March 2020; Accepted: 3 April 2020; Published: 4 April 2020 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, 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. Keywords: spirochetes; periplasmic flagella; motility; chemotaxis; molecular motor 1. Introduction Motility systems of living organisms are currently classified into 18 types [1]. Even when focusing on bacteria only, the motility is diverse when bacterial species are concerned [2]. A major motility form would be the flagella-dependent swimming well observed and described in Escherichia coli and Salmonella enterica, and these species have helical flagella extending to the cell exterior. Spirochetes, which are members of a group of gram-negative bacteria with a spiral or flat-wave cell body, also show flagella-dependent motility, but their flagella are hidden within the periplasmic space and are thus called periplasmic flagella (PFs). Externally flagellated bacteria are propelled by direct interaction of flagella and fluid, whereas spirochetes swim by rolling or undulation of a cell body driven by PFs rotation beneath the outer membrane. Physics difference results in an invalidation of applying the canonical model obtained from external flagella to spirochetal periplasmic flagella. This review article describes the motility of spirochetes while connecting it with the unique structures of their cell bodies and PFs. Taxonomically, the phylum Spirochaetae is classified into Leptospiraceae, Brachyspiraceae, Spirochaetaceae, and Brevinemataceae families, containing pathogenic species, for example, Leptospira interrogans (leptospirosis), Brachyspira hyodysenteriae (swine dysentery), Borrelia burgdorferi (Lyme disease), and Treponema pallidum (syphilis). As observed with other motile pathogens, spirochete motility is an essential virulence factor. Thus, the last part of this review discusses the involvement of motility in spirochetal pathogenicity. 2. Cell Structure A schematic of the basic structure shared among spirochete species is shown in Figure1a. The protoplasmic cylinder consists of a cytoplasm, a cytoplasmic membrane, and a peptidoglycan layer, Biomolecules 2020, 10, 550; doi:10.3390/biom10040550 www.mdpi.com/journal/biomolecules Biomolecules 2020, 10, 550 2 of 15 Biomolecules2. Cell Structure2020, 10, 550 2 of 16 A schematic of the basic structure shared among spirochete species is shown in Figure 1a. The protoplasmic cylinder consists of a cytoplasm, a cytoplasmic membrane, and a peptidoglycan layer, which is covered by the outer membrane. Each PF filament connects with a basal motor called the which is covered by the outer membrane. Each PF filament connects with a basal motor called the flagellar motor that is embedded in the cytoplasmic membrane and the peptidoglycan layer via a flagellar motor that is embedded in the cytoplasmic membrane and the peptidoglycan layer via a short, bent structure corresponding to the universal joint hook in the E. coli flagellar motor (details short, bent structure corresponding to the universal joint hook in the E. coli flagellar motor (details are described below) [3]. The morphologies of the cell body and the PF as well as the number of PFs are described below) [3]. The morphologies of the cell body and the PF as well as the number of PFs greatly differ among species, and those of three representative species are summarized in Table1. The greatly differ among species, and those of three representative species are summarized in Table 1. cell body of Borrelia spp. exhibits a flat-wave shape and contains 7~11 PFs long enough to overlap with The cell body of Borrelia spp. exhibits a flat-wave shape and contains 7~11 PFs long enough to overlap thosewith extending those extending from the from other the end other at theend centerat the ofcenter the cellof the body cell [ 4body–7]. Brachyspira [4–7]. Brachyspiraspp. appear spp. appear to have ato flat-wave have a bodyflat-wave because body of because their non-spiral, of their non-sp almostiral, straight almost configuration straight configuration observed inobserved swimming in cellsswimming [8], but nocells explicit [8], but evidence no explicit has evidence been reported. has beenBrachyspira reported.PFs Brachyspira overlap atPFs the overlap cell center, at the and cell so docenter, those and of Borrelia so do those[9]. The of Borrelia cell morphology [9]. The cell of morphologyLeptospira spp. of Leptospira is distinguished spp. is distinguished from the other from two spirochetesthe other bytwo a smallspirochetes cell width by a and small short cell wavelength width and [ 4short,10]. Thewavelength protoplasmic [4,10]. cylinder The protoplasmic of Leptospira (Figurecylinder1b,c) of isLeptospira relatively (Figure rigid, 1b maintaining and c) is relatively the helix parametersrigid, maintaining even during the helix swimming, parameters whereas even bothduring ends swimming, of the cell whereas body are both frequently ends of transformed,the cell body are as described frequently later transformed, [11–14]. Unlike as describedBorrelia laterand Brachyspira[11–14]. Unlike, PFs ofBorreliaLeptospira and Brachyspiraare too short, PFs to overlapof Leptospira [15]. are too short to overlap [15]. FigureFigure 1. 1.Spirochetal Spirochetal cellcell structure. ( (aa)) Schematics Schematics of of longitudinal longitudinal and and zoom-in zoom-in cross-section cross-section views views of ofthe the cell cell structure structure and and the the flagellar flagellar motor motor shared shared by by spirochete spirochete species; species; outer outer membrane membrane (OM), (OM), periplasmicperiplasmic flagellum flagellum (PF),(PF), peptidoglycanpeptidoglycan layer (PG), inner membrane (IM), (IM), cytoplasm cytoplasm (CP), (CP), and and protoplasmicprotoplasmic cylinder cylinder (PC) are are shown. shown. If readers If readers view view from from the hook the hookto the tomotor, the motor,the flagellar the flagellar motor motorrotates rotates in a counterclockwise in a counterclockwise (CCW) (CCW) direction direction at one pole at one of a pole single of cell, a single whereas cell, whereasthe motor the at another motor at anothercell pole cell rotates pole rotates in a clockwise in a clockwise (CW) (CW)direction. direction. (b) Dark-field (b) Dark-field micrograph micrograph of Leptospira of Leptospira biflexa biflexa. (c) . (cLongitudinal) Longitudinal slice slice image image obtained obtained by by cryo-electron cryo-electron tomography tomography of of L.L. biflexa biflexa (adapted(adapted from from [14] [14 with] with permissionpermission from from the the publisher). publisher). OM,OM, IM,IM, and PF are clearly visible, and and PGs PGs observed observed in in the the yellow yellow squaresquare are are indicated indicated by by yellow yellow dashed dashed lineslines inin thethe enlargedenlarged viewview (inset). Biomolecules 2020, 10, 550 3 of 16 Biomolecules 2020, 10, 550 3 of 15 Biomolecules 2020, 10, 550 3 of 15 Biomolecules 2020, 10, 550 3 of 15 Table 1.TableTable Comparison1.1. ComparisonComparison ofof thethe of cellcell structurestructure the cell andand thethe structure periplperiplasmicasmic flagella andflagella (PFs) the(PFs) amam periplasmicongong threethree spirochetespirochete flagella (PFs) among three spirochetespecies.species.Table species. 1. Comparison of the cell structure and the periplasmic flagella (PFs) among three spirochete species.Species Cell Body Parameters PF Species Cell Morphology Cell Body Parameters PF Ref. (Disease) Cell Morphology Length Width Wavelength Number Shape Overlap Proteins Ref. Species(Disease)Species LengthCell WBodyidth Parameters WavelengthCell Body Number Parameters Shape PFOverlap Proteins PF CellCell Morphology Morphology Left- Ref. Ref. (Disease)Borrelia(Disease) burgdorfer i Length W~0.3idth Wavelength Number ShapeLeft- Overlap ProteinsFlaA Borrelia burgdorferi Flat wave ~20 μm ~0.3Length ~2.8 μm Width 14~22 Wavelengthhanded Yes Number FlaA [4–7] Shape Overlap Proteins (Lyme disease) Flat wave ~20 μm μm ~2.8 μm 14~22 handedLeft- Yes FlaB [4–7] Borrelia burgdorferiBorrelia(Lyme burgdorferdisease) i μ~0.3m helix FlaBFlaA Left-handed FlaA Flat
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