PreprintCited by 4Bacterial Genetics and BiotechnologyAdvanced Electron Microscopy Techniques and ApplicationsBiochemical and Structural Characterization

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Curvature generation and engineering principles from Shewanella oneidensis multi-flagellin flagellum

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Preprint — published as 10.1021/acsnano.5c02744 · Paper page

Abstract

Motility driven by nanoscale flagella is vital to microbial survival and spread in fluid and structured environments. Absence of native flagellum structures, however, has limited our understanding of the mechanisms of microbial motility, hindering efforts to engineer microbe-based microbots for applications. Here, by cryogenic electron tomography (cryoET) and microscopy (cryoEM), we determined the structural basis of motility driven by the single flagellum anchored to one pole of Shewanella oneidensis MR-1 ( S. oneidensis ), an electrogenic bacterium commonly used in biotechnology. The structures of the curved flagellum, representing the conformation during motion, are captured, allowing delineation of molecular interactions among the subunits of its three components—filament, hook, and hook-filament junction. The structures of the filament, i.e., the propeller, reveal a varying composition of the flagellin isoforms FlaA and FlaB throughout the filament. Distinct inter-subunit interactions are identified at residues 129 and 134, which are the major determinants of functional differences in motility for the two isoforms. The hook—the universal joint—has a significantly larger curvature than that of the filament, despite both containing 11 curvature-defining conformers of their subunits. Transition between the propeller and universal joint is mediated by hook-filament junction, composed of 11 subunits of FlgK and FlgL, reconciling incompatibility between the filament and hook. Correlating these compositional and structural transitions with varying levels of curvature in flagellar segments reveals molecular mechanism enabling propulsive motility. Mechanistic understandings from S. oneidensis suggest engineering principles for nanoscale biomimetic systems. Graphic abstract:

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Metadata

Authors
Lou, Q., Fan, H., Liu, Y., Miller, J. F., Huang, Y., & Zhou, Z. H.
Affiliations
  • California NanoSystems Institute (US)
  • University of California, Los Angeles (US)
Corresponding author
Zhou, Z. Hong
Venue
ACS Nano
Publisher
openRxiv
Published
2025-02-08
Volume
19
Issue
28
Pages
25682-25696
ISSN
1936-0851 (ISSN-L)
OpenAlex
W4412107127
Cited by
4
References
1
Citations by year
2025: 4
FWCI
2.35
Type
journal article
Language
en
Open access
Locations
  • ACS Nano (publishedVersion, cc-by-nc-nd)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by)
Funders
  • National Science Foundation (1338135, 1548924)
  • National Institutes of Health (1s10od018111-01)
  • University of California, Los Angeles (DBI-1338135, DMR-1548924, 1S10OD018111)
  • National Institute of General Medical Sciences (R01GM071940)
  • Division of Materials Research (DMR1548924, 1548924)
  • California NanoSystems Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
Keywords
Shewanella oneidensis, bacterial flagellum, flagellar motility, flaA, flaB, hooks, propellers

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