Spatial organization of the bacterial chemotaxis system

Current Opinion in Microbiology

Volumn 9, Issue 6, 2006, Pages 619-624

  Kentner, David ^a   Sourjik, Victor ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL GROWTH; CELL DIVISION; CELLULAR DISTRIBUTION; CHEMORECEPTOR; CHEMOTAXIS; CLUSTER ANALYSIS; ESCHERICHIA COLI; EUKARYOTE; GENE AMPLIFICATION; NONHUMAN; PROKARYOTE; REVIEW; SENSORY SYSTEM; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; CHEMOTAXIS; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; MEMBRANE PROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); EUKARYOTA; PROKARYOTA;

EID: 33751213049     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2006.10.012     Document Type: Review

References (49)

1. Szurmant H., and Ordal G.W. Diversity in chemotaxis mechanisms among the bacteria and archaea. Microbiol Mol Biol Rev 68 (2004) 301-319
2. Baker M.D., Wolanin P.M., and Stock J.B. Signal transduction in bacterial chemotaxis. Bioessays 28 (2006) 9-22
3. Bourret R.B., and Stock A.M. Molecular information processing: lessons from bacterial chemotaxis. J Biol Chem 277 (2002) 9625-9628
4. Bren A., and Eisenbach M. How signals are heard during bacterial chemotaxis: protein-protein interactions in sensory signal propagation. J Bacteriol 182 (2000) 6865-6873
5. Parkinson J.S., Ames P., and Studdert C.A. Collaborative signaling by bacterial chemoreceptors. Curr Opin Microbiol 8 (2005) 116-121
6. Wadhams G.H., and Armitage J.P. Making sense of it all: bacterial chemotaxis. Nat Rev Mol Cell Biol 5 (2004) 1024-1037
7. Sourjik V. Receptor clustering and signal processing in E. coli chemotaxis. Trends Microbiol 12 (2004) 569-576
8. Gegner J.A., Graham D.R., Roth A.F., and Dahlquist F.W. Assembly of an MCP receptor, CheW, and kinase CheA complex in the bacterial chemotaxis signal transduction pathway. Cell 70 (1992) 975-982
9. Berg H.C., and Purcell E.M. Physics of chemoreception. Biophys J 20 (1977) 193-219
10. Maddock J.R., and Shapiro L. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259 (1993) 1717-1723
11. Sourjik V., and Berg H.C. Localization of components of the chemotaxis machinery of Escherichia coli using fluorescent protein fusions. Mol Microbiol 37 (2000) 740-751
12. Li M., and Hazelbauer G.L. Cellular stoichiometry of the components of the chemotaxis signaling complex. J Bacteriol 186 (2004) 3687-3694
13. Gestwicki J.E., Lamanna A.C., Harshey R.M., McCarter L.L., Kiessling L.L., and Adler J. Evolutionary conservation of methyl-accepting chemotaxis protein location in Bacteria and Archaea. J Bacteriol 182 (2000) 6499-6502
14. Kim K.K., Yokota H., and Kim S.H. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400 (1999) 787-792
15. Ames P., Studdert C.A., Reiser R.H., and Parkinson J.S. Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99 (2002) 7060-7065
16. Homma M., Shiomi D., and Kawagishi I. Attractant binding alters arrangement of chemoreceptor dimers within its cluster at a cell pole. Proc Natl Acad Sci USA 101 (2004) 3462-3467
17. Studdert C.A., and Parkinson J.S. Crosslinking snapshots of bacterial chemoreceptor squads. Proc Natl Acad Sci USA 101 (2004) 2117-2122
18. Studdert C.A., and Parkinson J.S. Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc Natl Acad Sci USA 102 (2005) 15623-15628. This study used crosslinking to follow the exchange dynamics of receptor dimers among trimers-of-dimers in vivo to demonstrate that receptor complexes are stabilized by the binding of CheA and CheW.
19. Shimizu T.S., Le Novere N., Levin M.D., Beavil A.J., Sutton B.J., and Bray D. Molecular model of a lattice of signalling proteins involved in bacterial chemotaxis. Nat Cell Biol 2 (2000) 792-796
20. Kentner D., Thiem S., Hildenbeutel M., and Sourjik V. Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 61 (2006) 407-417. This study used fluorescence microscopy to show that receptors form large complexes in vivo even in absence of CheA and CheW through interactions between their cytoplasmic domains. The study also demonstrates that fragments of CheA, including the P5 domain, can bind to receptor clusters independently of CheW.
21. Skidmore J.M., Ellefson D.D., McNamara B.P., Couto M.M., Wolfe A.J., and Maddock J.R. Polar clustering of the chemoreceptor complex in Escherichia coli occurs in the absence of complete CheA function. J Bacteriol 182 (2000) 967-973
22. Kim S.H., Wang W., and Kim K.K. Dynamic and clustering model of bacterial chemotaxis receptors: structural basis for signaling and high sensitivity. Proc Natl Acad Sci USA 99 (2002) 11611-11615
23. Park S.Y., Borbat P.P., Gonzalez-Bonet G., Bhatnagar J., Pollard A.M., Freed J.H., Bilwes A.M., and Crane B.R. Reconstruction of the chemotaxis receptor-kinase assembly. Nat Struct Mol Biol 13 (2006) 400-407. This article reports a structure of the cytoplasmic part of a T. maritima chemoreceptor and shows that this fragment forms an extended linear array, rather than a trimer-of-dimers in a crystal. In addition, the study uses pulsed electron spin resonance (ESR) to analyse the protein arrangement in the CheA-CheW complex and proposes a model of the cluster where receptor arrays are bridged by interactions between the P5 domains of CheA.
24. Ames P., and Parkinson J.S. Constitutively signaling fragments of Tsr, the Escherichia coli serine chemoreceptor. J Bacteriol 176 (1994) 6340-6348
25. Levit M.N., Grebe T.W., and Stock J.B. Organization of the receptor-kinase signaling array that regulates Escherichia coli chemotaxis. J Biol Chem 277 (2002) 36748-36754
26. Miller A.S., Kohout S.C., Gilman K.A., and Falke J.J. CheA kinase of bacterial chemotaxis: chemical mapping of four essential docking sites. Biochemistry 45 (2006) 8699-8711. This study used a chemical modification approach for a systematic mapping of CheA sites that are important for the ternary complex formation and kinase regulation.
27. Bilwes A.M., Alex L.A., Crane B.R., and Simon M.I. Structure of CheA, a signal-transducing histidine kinase. Cell 96 (1999) 131-141
28. Griswold I.J., Zhou H., Matison M., Swanson R.V., McIntosh L.P., Simon M.I., and Dahlquist F.W. The solution structure and interactions of CheW from Thermotoga maritima. Nat Struct Biol 9 (2002) 121-125
29. Sourjik V., and Berg H.C. Functional interactions between receptors in bacterial chemotaxis. Nature 428 (2004) 437-441. This study used fluorescence resonance energy transfer (FRET) to follow changes in the kinase activity in living cells upon attractant stimulation. It shows that the kinase regulation by receptors is highly cooperative and can be described by a classical MWC model of allosteric protein complexes.
30. Shiomi D., Yoshimoto M., Homma M., and Kawagishi I. Helical distribution of the bacterial chemoreceptor via colocalization with the Sec protein translocation machinery. Mol Microbiol 60 (2006) 894-906. Using time-lapse imaging to follow the expression of Tar-GFP, the authors demonstrate that newly expressed receptors are initially inserted into the lateral membrane along the Sec translocation machinery and only later re-localize to the pole.
31. Cabin-Flaman A., Ripoll C., Saier Jr. M.H., and Norris V. Hypothesis: chemotaxis in Escherichia coli results from hyper-structure dynamics. J Mol Microbiol Biotechnol 10 (2005) 1-14
32. Mileykovskaya E., and Dowhan W. Visualization of phospholipid domains in Escherichia coli by using the cardiolipin-specific fluorescent dye 10-N-nonyl acridine orange. J Bacteriol 182 (2000) 1172-1175
33. Maki N., Gestwicki J.E., Lake E.M., Kiessling L.L., and Adler J. Motility and chemotaxis of filamentous cells of Escherichia coli. J Bacteriol 182 (2000) 4337-4342
34. Wadhams G.H., Warren A.V., Martin A.C., and Armitage J.P. Targeting of two signal transduction pathways to different regions of the bacterial cell. Mol Microbiol 50 (2003) 763-770
35. Thompson S.R., Wadhams G.H., and Armitage J.P. The positioning of cytoplasmic protein clusters in bacteria. Proc Natl Acad Sci USA 103 (2006) 8209-8214. The authors show that during division cytoplasmic receptor clusters in R. sphaeroides are actively segregated from the middle of a mother cell to the mid-cell positions of daughter cells. This segregation process depends on a PpfA positioning factor that is homologous to bacterial DNA partitioning factors.
36. Wadhams G.H., Martin A.C., Warren A.V., and Armitage J.P. Requirements for chemotaxis protein localization in Rhodobacter sphaeroides. Mol Microbiol 58 (2005) 895-902
37. Lamanna A.C., Ordal G.W., and Kiessling L.L. Large increases in attractant concentration disrupt the polar localization of bacterial chemoreceptors. Mol Microbiol 57 (2005) 774-785
38. Shrout A.L., Montefusco D.J., and Weis R.M. Template-directed assembly of receptor signaling complexes. Biochemistry 42 (2003) 13379-13385
39. Liberman L., Berg H.C., and Sourjik V. Effect of chemoreceptor modification on assembly and activity of the receptor-kinase complex in Escherichia coli. J Bacteriol 186 (2004) 6643-6646
40. Lybarger S.R., Nair U., Lilly A.A., Hazelbauer G.L., and Maddock J.R. Clustering requires modified methyl-accepting sites in low-abundance but not high-abundance chemoreceptors of Escherichia coli. Mol Microbiol 56 (2005) 1078-1086
41. Shiomi D., Banno S., Homma M., and Kawagishi I. Stabilization of polar localization of a chemoreceptor via its covalent modifications and its communication with a different chemoreceptor. J Bacteriol 187 (2005) 7647-7654
42. Vaknin A., and Berg H.C. Single-cell FRET imaging of phosphatase activity in the Escherichia coli chemotaxis system. Proc Natl Acad Sci USA 101 (2004) 17072-17077
43. Vaknin A., and Berg H.C. Osmotic stress mechanically perturbs chemoreceptors in Escherichia coli. Proc Natl Acad Sci USA 103 (2006) 592-596. This study uses fluorescence polarization measurement of homo-FRET between Tar-YFP (yellow fluorescence protein) fusions to show that repellent responses to osmotic agents change spacing and/or orientation of receptor dimers in the cluster.
44. Gestwicki J.E., and Kiessling L.L. Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415 (2002) 81-84
45. Lai R.Z., Manson J.M., Bormans A.F., Draheim R.R., Nguyen N.T., and Manson M.D. Cooperative signaling among bacterial chemoreceptors. Biochemistry 44 (2005) 14298-14307. This study demonstrates cooperative regulation of CheA activity in the reconstituted ternary complexes in vitro.
46. Zimmer M.A., Szurmant H., Saulmon M.M., Collins M.A., Bant J.S., and Ordal G.W. The role of heterologous receptors in McpB-mediated signalling in Bacillus subtilis chemotaxis. Mol Microbiol 45 (2002) 555-568
47. Li G., and Weis R.M. Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100 (2000) 357-365
48. Jahreis K., Morrison T.B., Garzon A., and Parkinson J.S. Chemotactic signaling by an Escherichia coli CheA mutant that lacks the binding domain for phosphoacceptor partners. J Bacteriol 186 (2004) 2664-2672
49. Okumura H., Nishiyama S., Sasaki A., Homma M., and Kawagishi I. Chemotactic adaptation is altered by changes in the carboxy-terminal sequence conserved among the major methyl-accepting chemoreceptors. J Bacteriol 180 (1998) 1862-1868