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A bacterial surface layer protein exploits multistep crystallization for rapid self-assembly.

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Herrmann J, Li PN, Jabbarpour F, Chan ACK, Rajkovic I, Matsui T, Shapiro L, Smit J, Weiss TM, Murphy MEP, Wakatsuki S
OpenAccess logo Proc Natl Acad Sci U S A 117 388-394 (2020)
Cited: 8 times
EuropePMC logo PMID: 31848245

Abstract

Surface layers (S-layers) are crystalline protein coats surrounding microbial cells. S-layer proteins (SLPs) regulate their extracellular self-assembly by crystallizing when exposed to an environmental trigger. However, molecular mechanisms governing rapid protein crystallization in vivo or in vitro are largely unknown. Here, we demonstrate that the Caulobacter crescentus SLP readily crystallizes into sheets in vitro via a calcium-triggered multistep assembly pathway. This pathway involves 2 domains serving distinct functions in assembly. The C-terminal crystallization domain forms the physiological 2-dimensional (2D) crystal lattice, but full-length protein crystallizes multiple orders of magnitude faster due to the N-terminal nucleation domain. Observing crystallization using a time course of electron cryo-microscopy (Cryo-EM) imaging reveals a crystalline intermediate wherein N-terminal nucleation domains exhibit motional dynamics with respect to rigid lattice-forming crystallization domains. Dynamic flexibility between the 2 domains rationalizes efficient S-layer crystal nucleation on the curved cellular surface. Rate enhancement of protein crystallization by a discrete nucleation domain may enable engineering of kinetically controllable self-assembling 2D macromolecular nanomaterials.

Articles - 6p5t mentioned but not cited (1)

  1. A bacterial surface layer protein exploits multistep crystallization for rapid self-assembly. Herrmann J, Li PN, Jabbarpour F, Chan ACK, Rajkovic I, Matsui T, Shapiro L, Smit J, Weiss TM, Murphy MEP, Wakatsuki S. Proc Natl Acad Sci U S A 117 388-394 (2020)


Reviews citing this publication (1)

  1. S-Layer Ultrafiltration Membranes. Schuster B, Sleytr UB. Membranes (Basel) 11 275 (2021)

Articles citing this publication (6)

  1. Design of biologically active binary protein 2D materials. Ben-Sasson AJ, Watson JL, Sheffler W, Johnson MC, Bittleston A, Somasundaram L, Decarreau J, Jiao F, Chen J, Mela I, Drabek AA, Jarrett SM, Blacklow SC, Kaminski CF, Hura GL, De Yoreo JJ, Kollman JM, Ruohola-Baker H, Derivery E, Baker D. Nature 589 468-473 (2021)
  2. Structure and assembly of the S-layer in C. difficile. Lanzoni-Mangutchi P, Banerji O, Wilson J, Barwinska-Sendra A, Kirk JA, Vaz F, O'Beirne S, Baslé A, El Omari K, Wagner A, Fairweather NF, Douce GR, Bullough PA, Fagan RP, Salgado PS. Nat Commun 13 970 (2022)
  3. High-resolution mapping of metal ions reveals principles of surface layer assembly in Caulobacter crescentus cells. Herdman M, von Kügelgen A, Kureisaite-Ciziene D, Duman R, El Omari K, Garman EF, Kjaer A, Kolokouris D, Löwe J, Wagner A, Stansfeld PJ, Bharat TAM. Structure 30 215-228.e5 (2022)
  4. In vitro investigation of protein assembly by combined microscopy and infrared spectroscopy at the nanometer scale. Zhao X, Li D, Lu YH, Rad B, Yan C, Bechtel HA, Ashby PD, Salmeron MB. Proc Natl Acad Sci U S A 119 e2200019119 (2022)
  5. Nested Formation of Calcium Carbonate Polymorphs in a Bacterial Surface Membrane with a Graded Nanoconfinement: An Evolutionary Strategy to Ensure Bacterial Survival. Simon P, Pompe W, Gruner D, Sturm E, Ostermann K, Matys S, Vogel M, Rödel G. ACS Biomater Sci Eng 8 526-539 (2022)
  6. The Polygonal Cell Shape and Surface Protein Layer of Anaerobic Methane-Oxidizing Methylomirabilis lanthanidiphila Bacteria. Gambelli L, Mesman R, Versantvoort W, Diebolder CA, Engel A, Evers W, Jetten MSM, Pabst M, Daum B, van Niftrik L. Front Microbiol 12 766527 (2021)


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