Adapt locally and act globally: Strategy to maintain high chemoreceptor sensitivity in complex environments

Molecular Systems Biology

Volumn 7, Issue , 2011, Pages

  Lan, Ganhui ^a   Schulmeister, Sonja ^b   Sourjik, Victor ^b   Tu, Yuhai ^a  

^a IBM T J WATSON RESEARCH CENTER   (United States)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

bacterial chemotaxis; high sensitivity to multiple signals; methylation crosstalk; mixed receptor cluster; sensory adaptation

Indexed keywords

CHEBC PROTEIN; CHER PROTEIN; ESCHERICHIA COLI PROTEIN; RECEPTOR; SERINE; TAR RECEPTOR; TSR RECEPTOR; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; CELL SURFACE RECEPTOR; CHEMOTACTIC FACTOR; LIGAND; MEMBRANE PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BACTERIUM; CHEMORECEPTOR; CHEMOTAXIS; CONFORMATIONAL TRANSITION; ESCHERICHIA COLI; LOCAL ADAPTATION; MATHEMATICAL MODEL; METHYLATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ADAPTATION; BIOLOGICAL MODEL; COMPUTER SIMULATION; DRUG EFFECT; METABOLISM; PHYSIOLOGY; SENSITIVITY AND SPECIFICITY;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

ADAPTATION, PHYSIOLOGICAL; BACTERIAL PROTEINS; CHEMOTACTIC FACTORS; CHEMOTAXIS; COMPUTER SIMULATION; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LIGANDS; MEMBRANE PROTEINS; METHYLATION; MODELS, BIOLOGICAL; RECEPTORS, CELL SURFACE; SENSITIVITY AND SPECIFICITY; SIGNAL TRANSDUCTION;

EID: 79952722800     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb.2011.8     Document Type: Article

References (57)

1. Adler J (1976) The sensing of chemicalbybacteria. Sci Am 302: 40-47
2. Adler J, Tso WW (1974) Decision-making in bacteria: chemotactic response of Escherichia coli to conflicting stimuli. Science 184: 1292-2294
3. Alon U, Surette MG, Barkai N, Leibler S (1999) Robustness in bacterial chemotaxis. Nature 397: 168-171
4. Ames P, Studdert CA, Reiser RH, Parkinson JS (2002) Collaborative signaling by mixed chemoreceptor teams in Escherichia coli. Proc Natl Acad Sci USA 99: 7060-7065 (Pubitemid 34526255)
5. Amin DN, Hazelbauer GL (2010) The chemoreceptor dimer is the unit of conformational coupling and transmembrane signaling. JBacteriol 192: 1193
6. Antommattei FM, Munzner JB, Weis RM (2004) Ligand-specific activation of Escherichia coli chemoreceptor transmethylation. J Bacteriol 186: 7556-7563 (Pubitemid 39463719)
7. BarkaiN,LeiblerS (1997) Robustness insimplebio chemical networks. Nature 387: 913-917
8. Berg HC, Brown DA (1972) Chemotaxis in E. coli analysed by three dimensional tracking. Nature 239: 500-504
9. Berg HC, Tedesco PM (1975) Transient response to chemotactic stimuli in Escherichia coli. Proc Natl Acad Sci USA 72: 3235-3239
10. Bornhorst JA, Falke JJ (2000) Attractant regulation of the aspartate receptor-kinase complex: limited cooperative interactions between receptors and effects of the receptor modification state. Biochemistry 39: 9486-9493 (Pubitemid 30626338)
11. Boyd A, Simon MI (1980) Multiple electrophoretic forms of methyl-accepting chemotaxis proteins generated by stimulus-elicited methylation in Escherichia coli. JBacteriol 143: 809-815 (Pubitemid 10017652)
12. Bozorth RM (1993) Ferromagnetism. Piscataway, NJ, USA: Wiley-IEEE Press
13. Bray D, Duke T (2004) Conformational spread: the propagation of allosteric states in large multiprotein complexes. Annu Rev Biophys Biomol Struct 33: 53-73 (Pubitemid 38829951)
14. Bray D, Levin MD, Morton-Firth CJ (1998) Receptor clustering as a cellular mechanism to control sensitivity. Nature 393: 85-88 (Pubitemid 28240260)
15. Cluzel P, Surette M, Leibler S (2000) An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287:1652-1655 (Pubitemid 30127766)
16. Djordjevic S, Goudreau PN, Xu Q, Stock AM, West AH (1998) Structural basis for methylesterase CheB regulation by a phosphorylation-activated domain. Proc Natl Acad Sci USA 95: 1381-1386 (Pubitemid 28103400)
17. Dunten P, Koshland DE (1991) Tuning the responsiveness of a sensory receptor via covalent modification. J Biol Chem 266: 1491-1496 (Pubitemid 21908329)
18. Duke TAJ, Bray D (1999) Heightened sensitivity of a lattice of membrane of receptors. Proc Natl Acad Sci USA 96: 10104-10108 (Pubitemid 29422519)
19. Endres RG, Wingreen NS (2006) Precise adaptation in bacterial chemotaxis through 'assistance neighborhoods'. Proc Natl Acad Sci USA 103: 13040-13044 (Pubitemid 44338913)
20. Falke JJ, Bass RB, Butler SL, Chervitz SA, Danielson MA (1997) The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes. Annu Rev Cell Dev Biol 13: 457-512 (Pubitemid 28034533)
21. Falke JJ, Hazelbauer GL (2001) Transmembrane signaling in bacterial chemoreceptors. Trends Biochem Sci 26: 257-265 (Pubitemid 32289244)
22. Goldman JP, Levin MD, Bray D (2009) Signal amplification in a lattice of coupled protein kinases. Mol Biosyst 5: 1853-1859
23. Grebe TW, Stock J (1998) Bacterial chemotaxis: the five sensors of a bacterium. CurrBiol8: R154-R157 (Pubitemid 28111447)
24. Hazelbauer GL, Falke JJ, Parkinson JS (2008) Bacterial chemo-receptors: high-performance signaling in networked arrays. Trends Biochem Sci 33: 9-19
25. Hoch JA, Silhavy TJ (1995) Two-component signal transduction. Washington DC, USA: American Society for Microbiology
26. Kalinin Y, Neumann S, Sourjik V, Wu M (2010) Responses of Escherichia coli bacteria to two opposing chemoattractant gradients depend on the chemoreceptor ratio. J Bacteriol 192: 1796-1800
27. Kentner D, Sourjik V (2009) Dynamic map of protein interactions in the Escherichia coli chemotaxis pathway. Mol SystBiol 5: 238
28. Kentner D, Thiem S, Hildenbeutel M, Sourjik V (2006) Determinants of chemoreceptor cluster formation in Escherichia coli. Mol Microbiol 161: 407-417 (Pubitemid 44356572)
29. Keymer JE, Endres RG, Skoge M, Meir Y, Wingreen NS (2006) Chemosensing in Escherichia coli: two regimes of two-state receptors. Proc Natl Acad Sci USA 103: 1786-1791 (Pubitemid 43228771)
30. Khursigara CM, Wu X, Zhang P, Lefman J, Subramaniam S (2008) Role of HAMP domains in chemotaxis signaling by bacterial chemoreceptors. Proc Natl Acad Sci USA 105: 16555-16560
31. Kim KK, Yokota H, Kim SH (1999) Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400: 787-792 (Pubitemid 29399543)
32. Laub MT, Goulian M (2007) Specificity in two-component signal transduction pathways. Annu Rev Genet 41: 121-145
33. Li G, Weis RM (2000) Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100: 357-365 (Pubitemid 30353091)
34. Maddock JR, Shapiro L (1993) Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259: 1717-1723 (Pubitemid 23114656)
35. Mao H, Cremer PS, Manson MD (2003) A sensitive, versatile microfluidic assay for bacterial chemotaxis. Proc Natl Acad Sci USA 100: 5449-5454 (Pubitemid 36542725)
36. Mello BA, Shaw L, Tu Y (2004) Effects of receptor interaction in bacterial chemotaxis. Biophys J 87: 1578-1595 (Pubitemid 39167016)
37. Mello BA, Tu Y (2003a) Perfect and near-perfect adaptation in a model ofbacterial chemotaxis. Biophys J 84: 2943-2956 (Pubitemid 36531746)
38. Mello BA, Tu Y (2003b) Quantitative modeling of sensitivity in bacterial chemotaxis: the role of coupling among different chemoreceptor species. Proc Natl Acad Sci USA 100: 8223-8228 (Pubitemid 36842526)
39. Mello BA, Tu Y (2005) An allosteric model for heterogeneous receptor complexes: understanding bacterial chemotaxis responses to multiple stimuli. Proc Natl Acad Sci USA 102: 17354-17359 (Pubitemid 41740870)
40. Mello BA, Tu Y (2007) Effects of adaptation in maintaining high sensitivity over a wide range of backgrounds for Escherichia coli chemotaxis. Biophys J92: 2329-2337 (Pubitemid 46536416)
41. Mesibov R, Ordal GW, Adler J (1973) The range of attractant concentrations for bacterial chemotaxis and the threshold and size of response over this range: Weber law and related phenomena. J Gen Physiol 62: 203-223
42. Monod J, Wyman J, Changeux JP (1965) On the nature of allosteric transitions: a plausible model. J Mol Biol 12: 88-118
43. Morton-Firth CJ, Shimizu TS, Bray D (1999) A free-energy-based stochastic simulation of the tar receptor complex. JMol Biol 286: 1059-1074 (Pubitemid 29116676)
44. Neumann S, Hansen CH, Wingreen NS, Sourjik V (2010) Differences in signalling by directly and indirectly binding lignads in bacterial chemotaxis. EMBO J29: 3484-3495
45. Sanders DA, Koshland DE (1988) Receptor interactions through phosphorylation and methylation pathways in bacterial chemo-taxis. Proc Natl Acad Sci USA 85: 8425-8429
46. Shimizu TS, Aksenov SV, Bray D (2003) A spatially extended stochastic model of the bacterial chemotaxis signalling pathway. J Mol Biol 329: 291-309 (Pubitemid 36561585)
47. Shimizu TS, Tu Y Berg HC (2010) A modulargradient-sensing network for chemotaxis in E. coli revealed by responses to time-varying stimuli. Mol SystBiol 6: 382
48. Silverman M, Simon M (1977) Chemotaxis in Escherichia coli: methylation of che gene products. Proc Natl Acad Sci USA 74: 3317-3321 (Pubitemid 8177767)
49. Sims JJ, Cohen RE (2009) Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of rap80. Mol cell 33: 775-783
50. Sims JJ, Haririnia A, Dickinson BC, Fushman D, Cohen RE (2009) Avid interactions underlie the Lys63-linked polyubiquitin binding specificities observed for UBA domains. Nat Struct Mol Biol 16: 883-889
51. Sourjik V, Berg HC (2002) Receptor sensitivity in bacterial chemotaxis. Proc Natl Acad Sci USA 99: 123-127 (Pubitemid 34060327)
52. Sourjik V, Berg HC (2004) Functional interactions between receptors in bacterial chemotaxi. Nature 428: 437-441 (Pubitemid 38419690)
53. Stock AM, Robinson VL, Goudreau PN (2000) Two-component signal transduction. Annu Rev Biochem 69: 183-215
54. Studdert CA, Parkinson JS (2005) Insights into the organization and dynamics of bacterial chemoreceptor clusters through in vivo crosslinking studies. Proc Natl Acad Sci USA 102: 15623-15628 (Pubitemid 41528106)
55. Vaknin A, Berg HC (2007) Physical responses of bacterial chemo-receptors. JMolBiol 366: 1416-1423
56. Webre DJ, Wolanin PM, Stock JB (2003) Bacterial chemotaxis. Curr Biol 13: 47-49
57. Yi TM, Huang Y Simon MI, Doyle J (2000) Robust perfect adaptation in bacterial chemotaxis through integral feedback control. Proc Natl Acad Sci USA 97: 4649-4653 (Pubitemid 30238612)