In situ structures of periplasmic flagella reveal a distinct cytoplasmic ATPase complex in Borrelia burgdorferi

Periplasmic flagella are essential for the distinct morphology and motility of spirochetes. A flagella-specific Type III secretion system (fT3SS) composed of a membrane-bound export apparatus and a cytosolic ATPase complex is responsible for the assembly of the periplasmic flagella. Here, we combine cryo-electron tomography and mutagenesis approaches to characterize the fT3SS machine in the Lyme disease spirochete Borrelia burgdorferi. We define the fT3SS machine by systematically characterizing mutants lacking key component genes. We discover that a distinct cytosolic ATPase complex is attached to the flagellar C-ring through multiple spoke-like linkers. The ATPase complex not only strengthens structural rigidity of the C-ring, but also undergoes conformational changes in concert with flagellar rotation. Our studies provide structural framework to uncover the unique mechanisms underlying assembly and rotation of the periplasmic flagella and may provide the bases for the development of novel therapeutic strategies against several pathogenic spirochetes.

• Publication year

  2018

• Venue

  bioRxiv

• Publication date

  2018-04-17

• Fields of study

  Biology, Medicine, Chemistry

• Identifiers
  DOI 10.1101/303222
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar

• No claims are published for this paper.

• No concepts are published for this paper.

• Structure of the Core of the Type Three Secretion System Export Apparatus

  2018cited by this paper
• Type‐III secretion pore formed by flagellar protein FliP

  2018cited by this paper
• Molecular architecture of the sheathed polar flagellum in Vibrio alginolyticus

  2017cited by this paper
• In Situ Molecular Architecture of the Salmonella Type III Secretion Machine.

  2017cited by this paper
• Spirochetes flagellar collar protein FlbB has astounding effects in orientation of periplasmic flagella, bacterial shape, motility, and assembly of motors in Borrelia burgdorferi

  2016cited by this paper
• Spirochete flagella hook protein self-catalyze a lysinoalanine covalent cross-link for motility

  2016cited by this paper
• Diverse high-torque bacterial flagellar motors assemble wider stator rings using a conserved protein scaffold

  2016cited by this paper
• A novel flagellar sheath protein, FcpA, determines filament coiling, translational motility and virulence for the Leptospira spirochete

  2016cited by this paper
• The bacterial flagellar motor and its structural diversity.

  2015cited by this paper
• Type III secretion systems: the bacterial flagellum and the injectisome

  2015cited by this paper
• Visualization of the type III secretion sorting platform of Shigella flexneri

  2015cited by this paper
• Spirochetal motility and chemotaxis in the natural enzootic cycle and development of Lyme disease.

  2015cited by this paper
• Mutations in the Borrelia burgdorferi Flagellar Type III Secretion System Genes fliH and fliI Profoundly Affect Spirochete Flagellar Assembly, Morphology, Motility, Structure, and Cell Division

  2015cited by this paper
• Motor Rotation Is Essential for the Formation of the Periplasmic Flagellar Ribbon, Cellular Morphology, and Borrelia burgdorferi Persistence within Ixodes scapularis Tick and Murine Hosts

  2015cited by this paper
• Assembly dynamics and the roles of FliI ATPase of the bacterial flagellar export apparatus

  2014cited by this paper
• ATPase-Independent Type-III Protein Secretion in Salmonella enterica

  2014cited by this paper
• Molecular Architecture of the Bacterial Flagellar Motor in Cells

  2014cited by this paper
• Electron counting and beam-induced motion correction enable near atomic resolution single particle cryoEM

  2013cited by this paper
• Cryoelectron tomography reveals the sequential assembly of bacterial flagella in Borrelia burgdorferi

  2013cited by this paper
• Common and distinct structural features of Salmonella injectisome and flagellar basal body

  2013influential reference
• Motility Is Crucial for the Infectious Life Cycle of Borrelia burgdorferi

  2013cited by this paper
• Study of the Response Regulator Rrp1 Reveals Its Regulatory Role in Chitobiose Utilization and Virulence of Borrelia burgdorferi

  2013cited by this paper
• Three-Dimensional Structures of Pathogenic and Saprophytic Leptospira Species Revealed by Cryo-Electron Tomography

  2012cited by this paper
• Structure of Flagellar Motor Proteins in Complex Allows for Insights into Motor Structure and Switching

  2012influential reference
• Architecture of the major component of the type III secretion system export apparatus

  2012influential reference
• FlaA Proteins in Leptospira interrogans Are Essential for Motility and Virulence but Are Not Required for Formation of the Flagellum Sheath

  2012cited by this paper
• The unique paradigm of spirochete motility and chemotaxis.

  2012cited by this paper
• Interaction between FliJ and FlhA, Components of the Bacterial Flagellar Type III Export Apparatus

  2012cited by this paper
• Common architecture of the flagellar type III protein export apparatus and F- and V-type ATPases

  2011cited by this paper
• Assembly and stability of flagellar motor in Escherichia coli

  2011influential reference
• A Novel Gene Inactivation System Reveals Altered Periplasmic Flagellar Orientation in a Borrelia burgdorferi fliL Mutant

  2011cited by this paper
• Structural diversity of bacterial flagellar motors

  2011cited by this paper
• Fast tomographic reconstruction on multicore computers

  2011cited by this paper
• An energy transduction mechanism used in bacterial flagellar type III protein export

  2011cited by this paper
• Organization and coordinated assembly of the type III secretion export apparatus

  2010cited by this paper
• Bacterial nanomachines: the flagellum and type III injectisome.

  2010cited by this paper
• 3D visualization of HIV virions by cryoelectron tomography.

  2010cited by this paper
• Cellular architecture of Treponema pallidum: novel flagellum, periplasmic cone, and cell envelope as revealed by cryo electron tomography.

  2010cited by this paper
• Structure of the cytoplasmic domain of FlhA and implication for flagellar type III protein export

  2010cited by this paper
• Inactivation of a putative flagellar motor switch protein FliG1 prevents Borrelia burgdorferi from swimming in highly viscous media and blocks its infectivity

  2010cited by this paper
• Role of the C-Terminal Cytoplasmic Domain of FlhA in Bacterial Flagellar Type III Protein Export

  2010cited by this paper
• Use of the Cre-lox Recombination System To Investigate the lp54 Gene Requirement in the Infectious Cycle of Borrelia burgdorferi

  2010cited by this paper
• Tomographic subvolume alignment and subvolume classification applied to myosin V and SIV envelope spikes.

  2009cited by this paper
• Intact Flagellar Motor of Borrelia burgdorferi Revealed by Cryo-Electron Tomography: Evidence for Stator Ring Curvature and Rotor/C-Ring Assembly Flexion

  2009cited by this paper
• Roles of the extreme N‐terminal region of FliH for efficient localization of the FliH–FliI complex to the bacterial flagellar type III export apparatus

  2009cited by this paper
• The Flat-Ribbon Configuration of the Periplasmic Flagella of Borrelia burgdorferi and Its Relationship to Motility and Morphology

  2008cited by this paper
• Distinct roles of the FliI ATPase and proton motive force in bacterial flagellar protein export

  2008cited by this paper
• Energy source of flagellar type III secretion

  2008cited by this paper
• Isolation and characterization of chemotaxis mutants of the Lyme disease Spirochete Borrelia burgdorferi using allelic exchange mutagenesis, flow cytometry, and cell tracking.

  2007cited by this paper
• 3D reconstruction and processing of volumetric data in cryo-electron tomography.

  2007cited by this paper
• Structural similarity between the flagellar type III ATPase FliI and F1-ATPase subunits

  2007influential reference
• The FliN-FliH interaction mediates localization of flagellar export ATPase FliI to the C ring complex.

  2006cited by this paper
• Mutational Analysis of the Flagellar Rotor Protein FliN: Identification of Surfaces Important for Flagellar Assembly and Switching

  2006cited by this paper
• Organization of FliN Subunits in the Flagellar Motor of Escherichia coli

  2006cited by this paper
• In situ structure of the complete Treponema primitia flagellar motor

  2006cited by this paper
• Scalable molecular dynamics with NAMD

  2005cited by this paper
• FlhB Regulates Ordered Export of Flagellar Components via Autocleavage Mechanism*

  2005cited by this paper
• UCSF Chimera—A visualization system for exploratory research and analysis

  2004cited by this paper
• Analysis of the Cytoplasmic Domains of Salmonella FlhA and Interactions with Components of the Flagellar Export Machinery

  2004cited by this paper
• How bacteria assemble flagella.

  2003influential reference
• Interactions of FliJ with the Salmonella Type III Flagellar Export Apparatus

  2003cited by this paper
• Oligomerization and activation of the FliI ATPase central to bacterial flagellum assembly

  2003cited by this paper
• Interactions among membrane and soluble components of the flagellar export apparatus of Salmonella.

  2002cited by this paper
• Molecular dissection of Salmonella FliH, a regulator of the ATPase FliI and the type III flagellar protein export pathway

  2002cited by this paper
• Intergenic Suppression between the Flagellar MS Ring Protein FliF of Salmonella and FlhA, a Membrane Component of Its Export Apparatus

  2001cited by this paper
• The structure of the central stalk in bovine F1-ATPase at 2.4 Å resolution

  2000cited by this paper
• Borrelia burgdorferi periplasmic flagella have both skeletal and motility functions.

  2000cited by this paper
• Domain Structure of Salmonella FlhB, a Flagellar Export Component Responsible for Substrate Specificity Switching

  2000influential reference
• Enzymatic Characterization of FliI

  1996cited by this paper
• Computer visualization of three-dimensional image data using IMOD.

  1996cited by this paper
• Morphological pathway of flagellar assembly in Salmonella typhimurium.

  1992cited by this paper
• Molecular Architecture

  1953influential reference

• No citing papers are available for this paper.