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Protein Structures Forming the Shell of Primitive Bacterial Organelles

Science
5 Aug 2005
Vol 309, Issue 5736
pp. 936-938

Abstract

Bacterial microcompartments are primitive organelles composed entirely of protein subunits. Genomic sequence databases reveal the widespread occurrence of microcompartments across diverse microbes. The prototypical bacterial microcompartment is the carboxysome, a protein shell for sequestering carbon fixation reactions. We report three-dimensional crystal structures of multiple carboxysome shell proteins, revealing a hexameric unit as the basic microcompartment building block and showing how these hexamers assemble to form flat facets of the polyhedral shell. The structures suggest how molecular transport across the shell may be controlled and how structural variations might govern the assembly and architecture of these subcellular compartments.

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References and Notes

1
T. E. Jensen, C. C. Bowen, Proc. Iowa Acad. Sci.68, 89 (1961).
2
E. Gantt, S. F. Conti, J. Bacteriol.97, 1486 (1969).
3
J. M. Shively, G. L. Decker, J. W. Greenawalt, J. Bacteriol.96, 2138 (1970).
4
J. M. Shively, R. S. English, Can. J. Bot.69, 957 (1991).
5
J. M. Shively, F. Ball, D. H. Brown, R. E. Saunders, Science182, 584 (1973).
6
G. D. Price, J. R. Coleman, M. R. Badger, Plant Physiol.100, 784 (1992).
7
A. K.-C. So, G. S. Espie, Plant Mol. Biol.37, 205 (1998).
8
A. K.-C. So et al., J. Bacteriol.186, 623 (2004).
9
G. A. Codd, W. J. N. Marsden, Biol. Rev. Camb. Philos. Soc.59, 389 (1984).
10
G. D. Price, M. R. Badger, Can. J. Bot.69, 963 (1990).
11
G. C. Cannon et al., Appl. Environ. Microbiol.67, 5351 (2001).
12
G. C. Cannon, S. Heinhorst, C. E. Bradburne, J. M. Shively, Funct. Plant Biol.29, 175 (2002).
13
J. M. Shively et al., Can. J. Bot.76, 906 (1998).
14
E. Kofoid, C. Rappleye, I. Stojiljkovic, J. Roth, J. Bacteriol.181, 5317 (1999).
15
G. D. Havemann, T. A. Bobik, J. Bacteriol.185, 5086 (2003).
16
M. R. Badger, D. Hanson, G. D. Price, Funct. Plant Biol.29, 161 (2002).
17
L. Holm, C. Sander, J. Mol. Biol.233, 123 (1993).
18
J.-F. Gibrat, T. Madej, S. H. Bryant, Curr. Opin. Struct. Biol.6, 377 (1996).
19
P. Yuan et al., Nat. Struct. Biol.10, 264 (2003).
20
J. M. Diprose et al., EMBO J.20, 7229 (2001).
21
H. Naitow, J. Tang, M. Canady, R. B. Wickner, J. E. Johnson, Nat. Struct. Biol.9, 725 (2002).
22
D. L. D. Caspar, A. Klug, Cold Spring Harb. Symp. Quant. Biol.27, 1 (1962).
23
J. M. Hogle, M. Chow, D. J. Filman, Sci. Am.256, 42 (March 1987).
24
M. G. Rossmann, J. E. Johnson, Annu. Rev. Biochem.58, 533 (1989).
25
S. C. Harrison, Curr. Opin. Struct. Biol.5, 157 (1995).
26
J. E. Johnson, J. A. Speir, J. Mol. Biol.269, 665 (1997).
27
S. C. Harrison, Curr. Opin. Struct. Biol.11, 195 (2001).
28
T. Stehle, S. J. Gamblin, Y. Yan, S. C. Harrison, Structure4, 165 (1996).
29
C. San Martin et al., Nat. Struct. Biol.9, 756 (2002).
30
A. K. So et al., J. Bacteriol.186, 623 (2004).
31
N. Ban, P. Nissen, J. Hansen, P. B. Moore, T. A. Steitz, Science289, 905 (2000).
32
W. L. DeLano, www.pymol.org (2002).
33
We thank G. Cannon and M. Yeager for helpful discussions, D. Krogmann for the gift of Synechocystis sp. PCC 6803 genomic DNA, and J. Laidman and H. Adesiteyo for technical assistance. We also thank R. W. Roberson, W. F. J. Vermass, and A. van de Meene for providing transmission electron micrographs of Syn 6803 cells. C.A.K and T.O.Y acknowledge the U.S. Department of Agriculture, the National Institutes of Health, and the Office of Science Biological and Environmental Research Program, the U.S. Department of Energy. The coordinates and structure factors have been deposited in the Protein Data Bank with accession numbers 2A10 (CcmK4, Form 1); 2A18 (CcmK4, Form 2); and 2A1B (CcmK2).

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Information & Authors

Information

Published In

Science
Volume 309 | Issue 5736
5 August 2005

Submission history

Received: 11 April 2005
Accepted: 22 June 2005
Published in print: 5 August 2005

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Notes

Supporting Online Material
www.sciencemag.org/cgi/content/full/309/5736/936/DC1
Materials and Methods
SOM Text
Figs. S1 to S3
References and Notes

Authors

Affiliations

Cheryl A. Kerfeld
Molecular Biology Institute, University of California, Los Angeles (UCLA), Box 951570, Los Angeles, CA 90095, USA.
Life Sciences Core, UCLA, Box 160606, Los Angeles, CA 90095, USA.
UCLA–U.S. Department of Energy (DOE) Institute for Genomics and Proteomics, Box 951570, Los Angeles, CA 90095–1570, USA.
Michael R. Sawaya
Molecular Biology Institute, University of California, Los Angeles (UCLA), Box 951570, Los Angeles, CA 90095, USA.
Department of Chemistry and Biochemistry, UCLA, Box 951569, Los Angeles, CA 90095, USA.
UCLA–U.S. Department of Energy (DOE) Institute for Genomics and Proteomics, Box 951570, Los Angeles, CA 90095–1570, USA.
Shiho Tanaka
Molecular Biology Institute, University of California, Los Angeles (UCLA), Box 951570, Los Angeles, CA 90095, USA.
Chau V. Nguyen
Molecular Biology Institute, University of California, Los Angeles (UCLA), Box 951570, Los Angeles, CA 90095, USA.
Martin Phillips
Molecular Biology Institute, University of California, Los Angeles (UCLA), Box 951570, Los Angeles, CA 90095, USA.
Department of Chemistry and Biochemistry, UCLA, Box 951569, Los Angeles, CA 90095, USA.
Morgan Beeby
Molecular Biology Institute, University of California, Los Angeles (UCLA), Box 951570, Los Angeles, CA 90095, USA.
Department of Chemistry and Biochemistry, UCLA, Box 951569, Los Angeles, CA 90095, USA.
Todd O. Yeates* [email protected]
Molecular Biology Institute, University of California, Los Angeles (UCLA), Box 951570, Los Angeles, CA 90095, USA.
Department of Chemistry and Biochemistry, UCLA, Box 951569, Los Angeles, CA 90095, USA.
UCLA–U.S. Department of Energy (DOE) Institute for Genomics and Proteomics, Box 951570, Los Angeles, CA 90095–1570, USA.

Notes

*
To whom correspondence should be addressed. E-mail: [email protected]

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