Self-Organization of the Escherichia coli Chemotaxis Network Imaged with Super-Resolution Light Microscopy

被引:251
作者
Greenfield, Derek [1 ,2 ]
McEvoy, Ann L. [1 ]
Shroff, Hari [3 ]
Crooks, Gavin E. [2 ]
Wingreen, Ned S. [4 ]
Betzig, Eric [3 ]
Liphardt, Jan [1 ,2 ,5 ]
机构
[1] Univ Calif Berkeley, Biophys Grad Grp, Berkeley, CA 94720 USA
[2] Univ Calif Berkeley, Lawrence Berkeley Lab, Phys Biosci Div, Berkeley, CA 94720 USA
[3] Howard Hughes Med Inst, Ashburn, VA USA
[4] Princeton Univ, Dept Mol Biol, Princeton, NJ 08544 USA
[5] Univ Calif Berkeley, Dept Phys, Berkeley, CA 94720 USA
来源
PLOS BIOLOGY | 2009年 / 7卷 / 06期
基金
美国国家卫生研究院;
关键词
PHOTOACTIVATED LOCALIZATION MICROSCOPY; BACTERIAL CHEMOTAXIS; CHEMORECEPTOR COMPLEX; FLUORESCENT PROTEIN; CELL-DIVISION; SERINE CHEMOTAXIS; RECEPTOR; LOCATION; PROBES; SENSITIVITY;
D O I
10.1371/journal.pbio.1000137
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
The Escherichia coli chemotaxis network is a model system for biological signal processing. In E. coli, transmembrane receptors responsible for signal transduction assemble into large clusters containing several thousand proteins. These sensory clusters have been observed at cell poles and future division sites. Despite extensive study, it remains unclear how chemotaxis clusters form, what controls cluster size and density, and how the cellular location of clusters is robustly maintained in growing and dividing cells. Here, we use photoactivated localization microscopy (PALM) to map the cellular locations of three proteins central to bacterial chemotaxis (the Tar receptor, CheY, and CheW) with a precision of 15 nm. We find that cluster sizes are approximately exponentially distributed, with no characteristic cluster size. One-third of Tar receptors are part of smaller lateral clusters and not of the large polar clusters. Analysis of the relative cellular locations of 1.1 million individual proteins (from 326 cells) suggests that clusters form via stochastic self-assembly. The super-resolution PALM maps of E. coli receptors support the notion that stochastic self-assembly can create and maintain approximately periodic structures in biological membranes, without direct cytoskeletal involvement or active transport.
引用
收藏
页数:11
相关论文
共 56 条
[1]   CHEMOTAXIS IN BACTERIA [J].
ADLER, J .
ANNUAL REVIEW OF BIOCHEMISTRY, 1975, 44 :341-356
[2]   Collaborative signaling by mixed chemoreceptor teams in Escherichia coli [J].
Ames, P ;
Studdert, CA ;
Reiser, RH ;
Parkinson, JS .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2002, 99 (10) :7060-7065
[3]   Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants:: the Keio collection [J].
Baba, Tomoya ;
Ara, Takeshi ;
Hasegawa, Miki ;
Takai, Yuki ;
Okumura, Yoshiko ;
Baba, Miki ;
Datsenko, Kirill A. ;
Tomita, Masaru ;
Wanner, Barry L. ;
Mori, Hirotada .
MOLECULAR SYSTEMS BIOLOGY, 2006, 2 (1) :2006.0008
[4]   Signal transduction in bacterial chemotaxis [J].
Baker, MD ;
Wolanin, PM ;
Stock, JB .
BIOESSAYS, 2006, 28 (01) :9-22
[5]   Multicolor super-resolution imaging with photo-switchable fluorescent probes [J].
Bates, Mark ;
Huang, Bo ;
Dempsey, Graham T. ;
Zhuang, Xiaowei .
SCIENCE, 2007, 317 (5845) :1749-1753
[6]   PHYSICS OF CHEMORECEPTION [J].
BERG, HC ;
PURCELL, EM .
BIOPHYSICAL JOURNAL, 1977, 20 (02) :193-219
[7]   Receptor density balances signal stimulation and attenuation in membrane-assembled complexes of bacterial chemotaxis signaling proteins [J].
Besschetnova, Tatiana Y. ;
Montefusco, David J. ;
Asinas, Abdalin E. ;
Shrout, Anthony L. ;
Antommattei, Frances M. ;
Weis, Robert M. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2008, 105 (34) :12289-12294
[8]   Imaging intracellular fluorescent proteins at nanometer resolution [J].
Betzig, Eric ;
Patterson, George H. ;
Sougrat, Rachid ;
Lindwasser, O. Wolf ;
Olenych, Scott ;
Bonifacino, Juan S. ;
Davidson, Michael W. ;
Lippincott-Schwartz, Jennifer ;
Hess, Harald F. .
SCIENCE, 2006, 313 (5793) :1642-1645
[9]   Super-resolution imaging in live Caulobacter crescentus cells using photoswitchable EYFP [J].
Biteen, Julie S. ;
Thompson, Michael A. ;
Tselentis, Nicole K. ;
Bowman, Grant R. ;
Shapiro, Lucy ;
Moerner, W. E. .
NATURE METHODS, 2008, 5 (11) :947-949
[10]   Receptor clustering as a cellular mechanism to control sensitivity [J].
Bray, D ;
Levin, MD ;
Morton-Firth, CJ .
NATURE, 1998, 393 (6680) :85-88