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CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus

Nature Microbiology volume 2, Article number: 16222 (2017) Cite this article

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A Corrigendum to this article was published on 22 December 2016

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Abstract

Archaea use flagella known as archaella—distinct both in protein composition and structure from bacterial flagella—to drive cell motility, but the structural basis of this function is unknown. Here, we report an atomic model of the archaella, based on the cryo electron microscopy (cryoEM) structure of the Methanospirillum hungatei archaellum at 3.4 Å resolution. Each archaellum contains ∼61,500 archaellin subunits organized into a curved helix with a diameter of 10 nm and average length of 10,000 nm. The tadpole-shaped archaellin monomer has two domains, a β-barrel domain and a long, mildly kinked α-helix tail. Our structure reveals multiple post-translational modifications to the archaella, including six O-linked glycans and an unusual N-linked modification. The extensive interactions among neighbouring archaellins explain how the long but thin archaellum maintains the structural integrity required for motility-driving rotation. These extensive inter-subunit interactions and the absence of a central pore in the archaellum distinguish it from both the bacterial flagellum and type IV pili.

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Figure 1: CryoEM data and refinement.
Figure 2: Post-translational modification of the M. hungatei flagellin.
Figure 3: Subunit–subunit interactions.
Figure 4: Adjacent subunit interactions.
Figure 5: Comparison between the M. hungatei archaellin and a bacterial type IV pilin and flagellin.
Figure 6: Comparison among prokaryotic motility filaments.

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  • 14 July 2017

    In the PDF version of this article previously published, the year of publication provided in the footer of each page and in the 'How to cite' section was erroneously given as 2017, it should have been 2016. This error has now been corrected. The HTML version of the article was not affected.

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Acknowledgements

This project received support from National Institutes of Health grants GM071940 and AI094386, NIH/NCRR/NCATS UCLA CTSI grant UL1TR000124, from the UCLA-DOE Institute (DE-FC03-02ER6342) to R.P.G. and R.O.L., and NSF grants DMR-1548924 to Z.H.Z. and 1515843 to R.P.G. N.P. was supported in part by the NIH Biotechnology Training Grant Program (T32GM067555). P.G. was supported in part by an American Heart Association Western States Affiliates Postdoc Fellowship (13POST17340020). The authors acknowledge the use of instruments at the Electron Imaging Center for Nanomachines supported by UCLA and by instrumentation grants from NIH (1S10OD018111) and NSF (DBI-1338135). NIH support for mass spectrometry was provided by grant S10RR025600. The authors acknowledge computer time at the Extreme Science and Engineering Discovery Environment (XSEDE, grant MCB140140 to Z.H.Z.).

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Authors and Affiliations

  1. Department of Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles (UCLA), Los Angeles, 90095, California, USA

    Nicole Poweleit, Peng Ge, Robert P. Gunsalus & Z. Hong Zhou

  2. Electron Imaging Center for Nanomachines, California Nano Systems Institute, UCLA, Los Angeles (UCLA), Los Angeles, 90095, California, USA

    Nicole Poweleit, Peng Ge & Z. Hong Zhou

  3. Department of Chemistry and Biochemistry, UCLA, Los Angeles 90095, UCLA, Los Angeles (UCLA), Los Angeles, 90095, California, USA

    Hong H. Nguyen & Rachel R. Ogorzalek Loo

  4. The UCLA-DOE Institute, UCLA, Los Angeles, 90095, California, USA

    Robert P. Gunsalus

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Contributions

Z.H.Z. and R.P.G. designed the project. N.P., P.G., R.R.O.L. and H.H.N. performed the experiments and analysed the data. Z.H.Z., R.P.G. and N.P. wrote the paper. All authors contributed to editing the manuscript.

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Correspondence to Z. Hong Zhou.

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Supplementary information

Supplementary Information

Supplementary Video Legends 1–8, Supplementary Figures 1-9, Supplementary Tables 1–3. (PDF 2758 kb)

Supplementary Video 1

Overview of the M. hungatei cryoEM density map. (AVI 21147 kb)

Supplementary Video 2

Overview of the M. hungatei FlaB monomer model. (AVI 32286 kb)

Supplementary Video 3

Overview of the extra densities in the cryoEM map. (AVI 26432 kb)

Supplementary Video 4

Overview of inter-subunit interactions. (AVI 37145 kb)

Supplementary Video 5

Focus on inter-subunit hydrophobic interactions. (AVI 29729 kb)

Supplementary Video 6

Focus on inter-subunit ionic interactions. (AVI 11128 kb)

Supplementary Video 7

Comparison between a bacterial pilin, archaellin and bacterial flagellin. (AVI 17338 kb)

Supplementary Video 8

Comparison between protofilaments of bacterial pili, archaella and bacterial flagella. (AVI 11914 kb)

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Poweleit, N., Ge, P., Nguyen, H. et al. CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus. Nat Microbiol 2, 16222 (2017). https://doi.org/10.1038/nmicrobiol.2016.222

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