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Structural basis of enzyme encapsulation into a bacterial nanocompartment

Nature Structural & Molecular Biology volume 15, pages 939–947 (2008)Cite this article

Abstract

Compartmentalization is an important organizational feature of life. It occurs at varying levels of complexity ranging from eukaryotic organelles and the bacterial microcompartments, to the molecular reaction chambers formed by enzyme assemblies. The structural basis of enzyme encapsulation in molecular compartments is poorly understood. Here we show, using X-ray crystallographic, biochemical and EM experiments, that a widespread family of conserved bacterial proteins, the linocin-like proteins, form large assemblies that function as a minimal compartment to package enzymes. We refer to this shell-forming protein as 'encapsulin'. The crystal structure of such a particle from Thermotoga maritima determined at 3.1-Å resolution reveals that 60 copies of the monomer assemble into a thin, icosahedral shell with a diameter of 240 Å. The interior of this nanocompartment is lined with conserved binding sites for short polypeptide tags present as C-terminal extensions of enzymes involved in oxidative-stress response.

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Figure 1: Alignment of selected encapsulin proteins.
Figure 2: Structure of the T. maritima encapsulin.
Figure 3: Structural comparison of T. maritima encapsulin with P. furiosus PfV and gp5 of the HK97 virus.
Figure 4: Packaged proteins possess a C-terminal extension.
Figure 5: Packaging of oligomeric cargo proteins.
Figure 6: Schematic architectural and primary-structure organization of the different types of encapsulins.

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Acknowledgements

Crystallographic data were collected at the beamline X06SA at the Swiss Light Source (SLS). We are grateful to C. Schulze-Briese, E. Pohl and T. Tomizaki for their outstanding support at the SLS. We thank R. Brunisholz, P. Hunziker and Y. Auchli at the Functional Genomics Center Zurich for mass-spectrometric analysis, the Electron Microscopy Center Zurich (EMEZ) and Martin Beck for support with EM data collection, M. Müller, F. Voigts-Hoffmann and F. Imkamp for critically reading the manuscript and all members of the Ban and Weber-Ban laboratory for suggestions and discussions. D.B. was supported by a Federation of European Biochemical Societies long-term fellowship. This work was supported by the Swiss National Science Foundation (SNSF) (to N.B. and E.W.B.) and the National Center of Excellence in Research (NCCR) Structural Biology program of the SNSF (to N.B. and E.W.B.).

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Authors and Affiliations

  1. ETH Zurich, Institute of Molecular Biology and Biophysics, Schafmattstrasse 20, Zurich, 8093, Switzerland

    Markus Sutter, Daniel Boehringer, Eilika Weber-Ban & Nenad Ban

  2. Novartis Institutes for Biomedical Research, Novartis Pharma AG, Basel, 4056, Switzerland

    Sascha Gutmann

  3. ETH Zurich, Institute of Food Science and Nutrition, Schmelzbergstrasse 9, Zurich, 8092, Switzerland

    Susanne Günther & Martin J Loessner

  4. Molecular Biology of the Gene in Extremophiles Unit, Institute Pasteur, rue Docteur Roux 25, Paris, 75724, Cedex 15, France

    David Prangishvili

  5. Lehrstuhl für Mikrobiologie und Archaeenzentrum, Universität Regensburg, Universitätsstrasse 31, 93053, Regensburg, Germany

    Karl O Stetter

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Correspondence to Eilika Weber-Ban or Nenad Ban.

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Sutter, M., Boehringer, D., Gutmann, S. et al. Structural basis of enzyme encapsulation into a bacterial nanocompartment. Nat Struct Mol Biol 15, 939–947 (2008). https://doi.org/10.1038/nsmb.1473

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