Convergent evolution in the supercoiling of prokaryotic flagellar filaments

Kreutzberger, Mark A.; Sonani, Ravi R.; Liu, Junfeng; Chatterjee, Sharanya; Wang, Fengbin; Sebastian, Amanda L.; Biswas, Prabir Kumar; Ewing, Cheryl P.; Zheng, Weili; Poly, Frédéric; Frankel, Gad; Luisi, Ben F.; Calladine, C. R.; Krupovìč, Mart; Scharf, Birgit E.

doi:10.1016/j.cell.2022.08.009

Cited by 22 publications

(32 citation statements)

References 66 publications

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“…However, we were unable to find a homogeneous subset of segments from which we could generate a significantly higher-resolution helical reconstruction. We thus sought to use the asymmetric reconstruction approach as has been employed for other quasihelical filaments ( 34 , 35 ).…”

Section: Resultsmentioning

confidence: 99%

Tad and toxin-coregulated pilus structures reveal unexpected diversity in bacterial type IV pili

Sonani,

Sanchez,

Baumgardt

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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Type IV pili (T4P) are ubiquitous in both bacteria and archaea. They are polymers of the major pilin protein, which has an extended and protruding N-terminal helix, α1, and a globular C-terminal domain. Cryo-EM structures have revealed key differences between the bacterial and archaeal T4P in their C-terminal domain structure and in the packing and continuity of α1. This segment forms a continuous α-helix in archaeal T4P but is partially melted in all published bacterial T4P structures due to a conserved helix breaking proline at position 22. The tad (tight adhesion) T4P are found in both bacteria and archaea and are thought to have been acquired by bacteria through horizontal transfer from archaea. Tad pilins are unique among the T4 pilins, being only 40 to 60 residues in length and entirely lacking a C-terminal domain. They also lack the Pro22 found in all high-resolution bacterial T4P structures. We show using cryo-EM that the bacterial tad pilus fromCaulobacter crescentusis composed of continuous helical subunits that, like the archaeal pilins, lack the melted portion seen in other bacterial T4P and share the packing arrangement of the archaeal T4P. We further show that a bacterial T4P, theVibrio choleraetoxin coregulated pilus, which lacks Pro22 but is not in the tad family, has a continuous N-terminal α-helix, yet its α1 s are arranged similar to those in other bacterial T4P. Our results highlight the role of Pro22 in helix melting and support an evolutionary relationship between tad and archaeal T4P.

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Section: Resultsmentioning

confidence: 99%

Tad and toxin-coregulated pilus structures reveal unexpected diversity in bacterial type IV pili

Sonani,

Sanchez,

Baumgardt

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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“…Powerful methodological approaches to high-resolution analysis have helped to discover that symmetric supramolecular assemblies of many viruses, storage or transport cages 14 , cytoskeleton 40 – 42 , flagella 43 , 44 , amyloid fibers 45 and others can exist in structurally polymorphic states, with each type of self-assembly usually associated with a specific biological function. Structural polymorphism can also be applied to many recombinant VLPs, protein cages, and (artificial) peptide assemblies, providing a large repertoire of molecular platforms for vaccines, drug delivery systems, nanoreactors, biomaterials or nanomachines 14 , 19 , 21 , 46 – 48 .…”

Section: Discussionmentioning

confidence: 99%

From structural polymorphism to structural metamorphosis of the coat protein of flexuous filamentous potato virus Y

Kavčič,

Kežar,

Koritnik

et al. 2024

Commun Chem

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The structural diversity and tunability of the capsid proteins (CPs) of various icosahedral and rod-shaped viruses have been well studied and exploited in the development of smart hybrid nanoparticles. However, the potential of CPs of the wide-spread flexuous filamentous plant viruses remains to be explored. Here, we show that we can control the shape, size, RNA encapsidation ability, symmetry, stability and surface functionalization of nanoparticles through structure-based design of CP from potato virus Y (PVY). We provide high-resolution insight into CP-based self-assemblies, ranging from large polymorphic or monomorphic filaments to smaller annular, cubic or spherical particles. Furthermore, we show that we can prevent CP self-assembly in bacteria by fusion with a cleavable protein, enabling controlled nanoparticle formation in vitro. Understanding the remarkable structural diversity of PVY CP not only provides possibilities for the production of biodegradable nanoparticles, but may also advance future studies of CP’s polymorphism in a biological context.

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“…C. crescentus flagellins do not contain D2 or D3 domains as observed in other bacterial systems (26,30,31). Instead, the D1 domain serves as the surface exposed region of the Caulobacter flagellin monomer.…”

Section: Structurementioning

confidence: 90%

“…However, these studies assessed filaments containing point mutations which altered their flagellin packing and locked them into straightened forms (24,25). As cryo-EM data processing methods improve there is interest in understanding how interactions in non-straightened structures impacts the overall helical architecture of the filament (13,26,27).…”

Section: Introductionmentioning

confidence: 99%

Atomic-level architecture ofCaulobacter crescentusflagellar filaments provide evidence for multi-flagellin filament stabilization

Sanchez,

Montemayor,

Ploscariu

et al. 2023

Preprint

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Flagella are dynamic, ion-powered machines with assembly pathways that are optimized for efficient flagella production. In bacteria, dozens of genes are coordinated at specific times in the cell lifecycle to generate each component of the flagellum. This is the case forCaulobacter crescentus, but little is known about why this species encodes six different flagellin genes. Furthermore, little is known about the benefits multi-flagellin species possess over single flagellin species, if any, or what molecular properties allow for multi-flagellin filaments to assemble. Here we present an in-depth analysis of several single flagellin filaments fromC. crescentus,including an extremely well-resolved structure of a bacterial flagellar filament. We highlight key molecular interactions that differ between each bacterial strain and speculate how these interactions may alleviate or impose helical strain on the overall architecture of the filament. We detail conserved residues within the flagellin subunit that allow for the synthesis of multi-flagellin filaments. We further comment on how these molecular differences impact bacterial motility and highlight how no single flagellin filament achieves wild-type levels of motility, suggestingC. crescentushas evolved to produce a filament optimized for motility comprised of six flagellins. Finally, we highlight an ordered arrangement of glycosylation sites on the surface of the filaments and speculate how these sites may protect the β-hairpin located on the surface exposed domain of the flagellin subunit.

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Convergent evolution in the supercoiling of prokaryotic flagellar filaments

Cited by 22 publications

References 66 publications

Tad and toxin-coregulated pilus structures reveal unexpected diversity in bacterial type IV pili

Tad and toxin-coregulated pilus structures reveal unexpected diversity in bacterial type IV pili

From structural polymorphism to structural metamorphosis of the coat protein of flexuous filamentous potato virus Y

Atomic-level architecture ofCaulobacter crescentusflagellar filaments provide evidence for multi-flagellin filament stabilization

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