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Three-Dimensional Electron Microscopic Imaging of Membrane Invaginations in Escherichia coli Overproducing the Chemotaxis Receptor Tsr

Jonathan Lefman,^1, Peijun Zhang,^1, Teruhisa Hirai,¹ Robert M. Weis,^1,2 Jemma Juliani,¹ Donald Bliss,¹ Martin Kessel,¹ Erik Bos,³ Peter J. Peters,³ and Sriram Subramaniam^1*

Laboratory of Cell Biology, National Cancer Institute, National Institutes of Health, Bethesda, Maryland 20817,¹ Department of Chemistry, University of Massachusetts, Amherst, Massachusetts 01003,² Division of Tumor Biology, The Netherlands Cancer Institute, Amsterdam, The Netherlands³

Received 24 December 2003/ Accepted 30 March 2004

Electron tomography is a powerful method for determining the three-dimensional structures of large macromolecular assemblies, such as cells, organelles, and multiprotein complexes, when crystallographic averaging methods are not applicable. Here we used electron tomographic imaging to determine the molecular architecture of Escherichia coli cells engineered to overproduce the bacterial chemotaxis receptor Tsr. Tomograms constructed from fixed, cryosectioned cells revealed that overproduction of Tsr led to formation of an extended internal membrane network composed of stacks and extended tubular structures. We present an interpretation of the tomogram in terms of the packing arrangement of Tsr using constraints derived from previous X-ray and electron-crystallographic studies of receptor clusters. Our results imply that the interaction between the cytoplasmic ends of Tsr is likely to stabilize the presence of the membrane networks in cells overproducing Tsr. We propose that membrane invaginations that are potentially capable of supporting axial interactions between receptor clusters in apposing membranes could also be present in wild-type E. coli and that such receptor aggregates could play an important role in signal transduction during bacterial chemotaxis.

J.L. and P.Z. contributed equally to this work.

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