Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr

Jonathan Lefman, Peijun Zhang, Teruhisa Hirai, Robert M. Weis, Jemma Juliani, Donald Frank Bliss, Martin Kessel, Erik Bos, Peter J. Peters, Sriram Subramaniam

Research output: Contribution to journalArticle

Abstract

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.

Original languageEnglish (US)
Pages (from-to)5052-5061
Number of pages10
JournalJournal of Bacteriology
Volume186
Issue number15
DOIs
StatePublished - Aug 2004
Externally publishedYes

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Chemotaxis
Electrons
Escherichia coli
Membranes
Electron Microscope Tomography
Multiprotein Complexes
Organelles
Signal Transduction
X-Rays

ASJC Scopus subject areas

  • Applied Microbiology and Biotechnology
  • Immunology

Cite this

Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr. / Lefman, Jonathan; Zhang, Peijun; Hirai, Teruhisa; Weis, Robert M.; Juliani, Jemma; Bliss, Donald Frank; Kessel, Martin; Bos, Erik; Peters, Peter J.; Subramaniam, Sriram.

In: Journal of Bacteriology, Vol. 186, No. 15, 08.2004, p. 5052-5061.

Research output: Contribution to journalArticle

Lefman, J, Zhang, P, Hirai, T, Weis, RM, Juliani, J, Bliss, DF, Kessel, M, Bos, E, Peters, PJ & Subramaniam, S 2004, 'Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr', Journal of Bacteriology, vol. 186, no. 15, pp. 5052-5061. https://doi.org/10.1128/JB.186.15.5052-5061.2004
Lefman, Jonathan ; Zhang, Peijun ; Hirai, Teruhisa ; Weis, Robert M. ; Juliani, Jemma ; Bliss, Donald Frank ; Kessel, Martin ; Bos, Erik ; Peters, Peter J. ; Subramaniam, Sriram. / Three-dimensional electron microscopic imaging of membrane invaginations in Escherichia coli overproducing the chemotaxis receptor Tsr. In: Journal of Bacteriology. 2004 ; Vol. 186, No. 15. pp. 5052-5061.
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AU - Weis, Robert M.

AU - Juliani, Jemma

AU - Bliss, Donald Frank

AU - Kessel, Martin

AU - Bos, Erik

AU - Peters, Peter J.

AU - Subramaniam, Sriram

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