The Heterogeneous Motility of the Lyme Disease Spirochete in Gelatin Mimics Dissemination through Tissue

Harman, Michael W.

doi:10.1016/j.bpj.2011.11.829

Cited by 25 publications

(40 citation statements)

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“…Borrelia burgdorferi is the causative agent of Lyme disease, which is the most prevalent tick‐borne disease in the United States and Europe (Burgdorfer et al, ; Sanchez, Vannier, Wormser, & Hu, ; Steere et al, , ). Previous studies have unveiled that motility plays a critical role in the pathogenicity of B. burgdorferi (e.g., dissemination, immune evasion, and transmission between the tick vector and mammalian hosts during the infectious cycle) (Dunham‐Ems et al, ; Harman et al, ; Li, Xu, Zhang, & Liang, ; Motaleb et al, ; Sultan et al, ). Due to its medical importance, genetic tractability and small cell diameter suitable for cryo‐electron tomography (cryo‐ET) analyses, B. burgdorferi has emerged as a model organism to study the regulation, structure and assembly of PF, motility, as well as chemotaxis in spirochetes (Brisson, Drecktrah, Eggers, & Samuels, ; Charon et al, ; Liu et al, ; Rosa et al, ; Zhao et al, ).…”

Section: Introductionmentioning

confidence: 99%

FlhF regulates the number and configuration of periplasmic flagella in Borrelia burgdorferi

Zhang

Cantalano

et al. 2020

Molecular Microbiology

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The Lyme disease bacterium Borrelia burgdorferi has 7–11 periplasmic flagella (PF) that arise from the cell poles and extend toward the midcell as a flat‐ribbon, which is distinct from other bacteria. FlhF, a signal recognition particle (SRP)‐like GTPase, has been found to regulate the flagellar number and polarity; however, its role in B. burgdorferi remains unknown. B. burgdorferi has an FlhF homolog (BB0270). Structural and biochemical analyses show that BB0270 has a similar structure and enzymatic activity as its counterparts from other bacteria. Genetics and cryo‐electron tomography studies reveal that deletion of BB0270 leads to mutant cells that have less PF (4 ± 2 PF per cell tip) and fail to form a flat‐ribbon, indicative of a role of BB0270 in the control of PF number and configuration. Mechanistically, we demonstrate that BB0270 localizes at the cell poles and controls the number and position of PF via regulating the flagellar protein stability and the polar localization of the MS‐ring protein FliF. Our study not only provides the detailed characterizations of BB0270 and its profound impacts on flagellar assembly, morphology and motility in B. burgdorferi, but also unveils mechanistic insights into how spirochetes control their unique flagellar patterns.

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Section: Introductionmentioning

confidence: 99%

FlhF regulates the number and configuration of periplasmic flagella in Borrelia burgdorferi

Zhang

Cantalano

et al. 2020

Molecular Microbiology

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“…Motion analysis of a swine intestinal spirochete, Brachyspira pilosicoli, showed that v/f increased in polyvinylpyrrolidone solutions but did not increase in Ficoll solutions (17). Also, Harman et al (20) investigated the motion and morphological parameters of Bo. burgdorferi, showing that the cells translate without slippage in gelatin solutions.…”

Section: Kinematic Parameters Of Swimming Leptospiramentioning

confidence: 99%

Direct Measurement of Helical Cell Motion of the Spirochete Leptospira

Nakamura

Leshansky

Magariyama

et al. 2014

Biophysical Journal

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Leptospira are spirochete bacteria distinguished by a short-pitch coiled body and intracellular flagella. Leptospira cells swim in liquid with an asymmetric morphology of the cell body; the anterior end has a long-pitch spiral shape (S-end) and the posterior end is hook-shaped (H-end). Although the S-end and the coiled cell body called the protoplasmic cylinder are thought to be responsible for propulsion together, most observations on the motion mechanism have remained qualitative. In this study, we analyzed the swimming speed and rotation rate of the S-end, protoplasmic cylinder, and H-end of individual Leptospira cells by one-sided dark-field microscopy. At various viscosities of media containing different concentrations of Ficoll, the rotation rate of the S-end and protoplasmic cylinder showed a clear correlation with the swimming speed, suggesting that these two helical parts play a central role in the motion of Leptospira. In contrast, the H-end rotation rate was unstable and showed much less correlation with the swimming speed. Forces produced by the rotation of the S-end and protoplasmic cylinder showed that these two helical parts contribute to propulsion at nearly equal magnitude. Torque generated by each part, also obtained from experimental motion parameters, indicated that the flagellar motor can generate torque >4000 pN nm, twice as large as that of Escherichia coli. Furthermore, the S-end torque was found to show a markedly larger fluctuation than the protoplasmic cylinder torque, suggesting that the unstable H-end rotation might be mechanically related to changes in the S-end rotation rate for torque balance of the entire cell. Variations in torque at the anterior and posterior ends of the Leptospira cell body could be transmitted from one end to the other through the cell body to coordinate the morphological transformations of the two ends for a rapid change in the swimming direction.

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“…Examples of these include bacteria forming biofilms composed of bacteria-produced extracellular polymeric substances (Hall-Stoodley, Costerton & Stoodley 2004), spermatozoa swimming through cervical mucus in the mammalian female reproductive tract (Suarez & Pacey 2006), Helicobacter pylori colonizing the mucus layer covering the stomach (Montecucco & Rappuoli 2001) and Borrelia burgdorferi penetrating the connective tissues in skin (Harman et al 2012). In marine environments, bacteria abundance and productivity are elevated within aggregates mainly composed of transparent exopolymer particles referred to as oceanic gel (Smith et al 1992).…”

Section: Introductionmentioning

confidence: 99%

Undulatory swimming in non-Newtonian fluids

Ardekani

2015

J. Fluid Mech.

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We numerically investigate the effects of non-Newtonian fluid properties, including shear thinning and elasticity, on the locomotion of Taylor's swimming sheet with arbitrary amplitude. Our results show that elasticity hinders the swimming speed, but a shear-thinning viscosity in the absence of elasticity enhances the speed. The combination of the two effects, modelled using a Giesekus constitutive equation, hinders the swimming speed. We find that the swimming speed of an infinitely long waving sheet in an inelastic shear-thinning fluid has a maximum, whose value depends on the sheet undulation amplitude and the fluid rheological properties. The power consumption, on the other hand, follows a universal scaling law.

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The Heterogeneous Motility of the Lyme Disease Spirochete in Gelatin Mimics Dissemination through Tissue

Cited by 25 publications

References 0 publications

FlhF regulates the number and configuration of periplasmic flagella in Borrelia burgdorferi

FlhF regulates the number and configuration of periplasmic flagella in Borrelia burgdorferi

Direct Measurement of Helical Cell Motion of the Spirochete Leptospira

Undulatory swimming in non-Newtonian fluids

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