Dynamics of the Serine Chemoreceptor in the Escherichia Coli Inner Membrane: a High-speed Single-molecule Tracking Study

Overview

Journal Biophys J

Publisher Cell Press

Specialty Biophysics

Date 2014 Jan 14

PMID 24411246

Citations 18

Authors

Dongmyung Oh

Yang Yu

Hochan Lee

Barry L Wanner

Ken Ritchie

Affiliations

Soon will be listed here.

Abstract

We investigated the mobility of the polar localized serine chemoreceptor, Tsr, labeled by the fluorescent protein Venus in the inner membrane of live Escherichia coli cells at observation rates up to 1000 Hz. A fraction (7%) of all Tsr molecules shows free diffusion over the entire cell surface with an average diffusion coefficient of 0.40 ± 0.01 μm(2) s(-1). The remaining molecules were found to be ultimately confined in compartments of size 290 ± 15 nm and showed restricted diffusion at an inner barrier found at 170 ± 10 nm. At the shortest length-scales (<170 nm), all Tsr molecules diffuse equally. Disruption of the cytoskeleton and rounding of the cells resulted in an increase in the mobile fraction of Tsr molecules and a fragmenting of the previously polar cluster of Tsr consistent with a curvature-based mechanism of Tsr cluster maintenance.

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References

Kenkre V, Giuggioli L, Kalay Z . Molecular motion in cell membranes: analytic study of fence-hindered random walks. Phys Rev E Stat Nonlin Soft Matter Phys. 2008; 77(5 Pt 1):051907. DOI: 10.1103/PhysRevE.77.051907. View

Ritchie K, Kusumi A . Single-particle tracking image microscopy. Methods Enzymol. 2003; 360:618-34. DOI: 10.1016/s0076-6879(03)60131-x. View

Ames P, Studdert C, Reiser R, Parkinson J . Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci U S A. 2002; 99(10):7060-5. PMC: 124528. DOI: 10.1073/pnas.092071899. View

Deich J, Judd E, McAdams H, Moerner W . Visualization of the movement of single histidine kinase molecules in live Caulobacter cells. Proc Natl Acad Sci U S A. 2004; 101(45):15921-6. PMC: 528753. DOI: 10.1073/pnas.0404200101. View

Iwai N, Nagai K, Wachi M . Novel S-benzylisothiourea compound that induces spherical cells in Escherichia coli probably by acting on a rod-shape-determining protein(s) other than penicillin-binding protein 2. Biosci Biotechnol Biochem. 2003; 66(12):2658-62. DOI: 10.1271/bbb.66.2658. View

Niu L, Yu J . Investigating intracellular dynamics of FtsZ cytoskeleton with photoactivation single-molecule tracking. Biophys J. 2008; 95(4):2009-16. PMC: 2483766. DOI: 10.1529/biophysj.108.128751. View

Haldimann A, Wanner B . Conditional-replication, integration, excision, and retrieval plasmid-host systems for gene structure-function studies of bacteria. J Bacteriol. 2001; 183(21):6384-93. PMC: 100134. DOI: 10.1128/JB.183.21.6384-6393.2001. View

Oh D, Ogiue-Ikeda M, Jadwin J, Machida K, Mayer B, Yu J . Fast rebinding increases dwell time of Src homology 2 (SH2)-containing proteins near the plasma membrane. Proc Natl Acad Sci U S A. 2012; 109(35):14024-9. PMC: 3435163. DOI: 10.1073/pnas.1203397109. View

Kumar M, Mommer M, Sourjik V . Mobility of cytoplasmic, membrane, and DNA-binding proteins in Escherichia coli. Biophys J. 2010; 98(4):552-9. PMC: 2820653. DOI: 10.1016/j.bpj.2009.11.002. View

10.

Mullineaux C, Nenninger A, Ray N, Robinson C . Diffusion of green fluorescent protein in three cell environments in Escherichia coli. J Bacteriol. 2006; 188(10):3442-8. PMC: 1482841. DOI: 10.1128/JB.188.10.3442-3448.2006. View

11.

Katsuki T, Ailani D, Hiramoto M, Hiromi Y . Intra-axonal patterning: intrinsic compartmentalization of the axonal membrane in Drosophila neurons. Neuron. 2009; 64(2):188-99. DOI: 10.1016/j.neuron.2009.08.019. View

12.

Ritchie K, Shan X, Kondo J, Iwasawa K, Fujiwara T, Kusumi A . Detection of non-Brownian diffusion in the cell membrane in single molecule tracking. Biophys J. 2004; 88(3):2266-77. PMC: 1305276. DOI: 10.1529/biophysj.104.054106. View

13.

Biteen J, Goley E, Shapiro L, Moerner W . Three-dimensional super-resolution imaging of the midplane protein FtsZ in live Caulobacter crescentus cells using astigmatism. Chemphyschem. 2012; 13(4):1007-12. PMC: 3712621. DOI: 10.1002/cphc.201100686. View

14.

Kusumi A, Sako Y, Yamamoto M . Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells. Biophys J. 1993; 65(5):2021-40. PMC: 1225938. DOI: 10.1016/S0006-3495(93)81253-0. View

15.

Kim S, Gitai Z, Kinkhabwala A, Shapiro L, Moerner W . Single molecules of the bacterial actin MreB undergo directed treadmilling motion in Caulobacter crescentus. Proc Natl Acad Sci U S A. 2006; 103(29):10929-34. PMC: 1544151. DOI: 10.1073/pnas.0604503103. View

16.

English B, Hauryliuk V, Sanamrad A, Tankov S, Dekker N, Elf J . Single-molecule investigations of the stringent response machinery in living bacterial cells. Proc Natl Acad Sci U S A. 2011; 108(31):E365-73. PMC: 3150888. DOI: 10.1073/pnas.1102255108. View

17.

Maddock J, Shapiro L . Polar location of the chemoreceptor complex in the Escherichia coli cell. Science. 1993; 259(5102):1717-23. DOI: 10.1126/science.8456299. View

18.

Lill Y, Kaserer W, Newton S, Lill M, Klebba P, Ritchie K . Single-molecule study of molecular mobility in the cytoplasm of Escherichia coli. Phys Rev E Stat Nonlin Soft Matter Phys. 2012; 86(2 Pt 1):021907. DOI: 10.1103/PhysRevE.86.021907. View

19.

Fujiwara T, Ritchie K, Murakoshi H, Jacobson K, Kusumi A . Phospholipids undergo hop diffusion in compartmentalized cell membrane. J Cell Biol. 2002; 157(6):1071-81. PMC: 2174039. DOI: 10.1083/jcb.200202050. View

20.

Greenfield D, McEvoy A, Shroff H, Crooks G, Wingreen N, Betzig E . Self-organization of the Escherichia coli chemotaxis network imaged with super-resolution light microscopy. PLoS Biol. 2009; 7(6):e1000137. PMC: 2691949. DOI: 10.1371/journal.pbio.1000137. View