Structure of bacterial cytoplasmic chemoreceptor arrays and implications for chemotactic signaling

eLife

Volumn 2014, Issue 3, 2014, Pages

  Briegel, Ariane ^a   Ladinsky, Mark S ^a   Oikonomou, Catherine ^b   Jones, Christopher W ^c   Harris, Michael J ^d   Fowler, Daniel J ^d,e   Chang, Yi Wei ^b   Thompson, Lynmarie K ^d   Armitage, Judith P ^c   Jensen, Grant J ^a,b  

^a California Institute of Technology   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d UNIVERSITY OF MASSACHUSETTS   (United States)

^e UNIVERSITY OF VERMONT   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BACTERIAL CYTOPLASMIC CHEMORECEPTOR; BACTERIAL STRAIN; BACTERIUM; CHEMOTAXIS; CYTOLYSIS ASSAY; CYTOPLASMIC ARRAY; ELECTRON CRYOTOMOGRAPHY; ELECTRON TOMOGRAPHY; ENZYME ACTIVITY; FREEZE DRYING; IMAGE ANALYSIS; IMMUNOELECTRON MICROSCOPY; IMMUNOGOLD LABELING; MICROSCOPY; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN MICROARRAY; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; RHODOBACTER SPHAEROIDES; SENSORY RECEPTOR; SIGNAL TRANSDUCTION; TRANSMEMBRANE ARRAY; VIBRIO CHOLERAE; CHEMORECEPTOR CELL; CYTOPLASM; DIMERIZATION; METABOLISM; PROCEDURES; TOMOGRAPHY;

CHEMORECEPTOR CELLS; CHEMOTAXIS; CYTOPLASM; DIMERIZATION; RHODOBACTER SPHAEROIDES; SIGNAL TRANSDUCTION; TOMOGRAPHY; VIBRIO CHOLERAE;

EID: 84898763141     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02151     Document Type: Article

References (58)

1. Agulleiro JI, Fernandez JJ. 2011. Fast tomographic reconstruction on multicore computers. Bioinformatics 27:582-583. doi: 10.1093/bioinformatics/btq692.
2. Alexander RP, Zhulin IB. 2007. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proceedings of the National Academy of Sciences of the United States of America 104:2885-2890. doi: 10.1073/pnas.0609359104.
3. Amin DN, Hazelbauer GL. 2012. Influence of membrane lipid composition on a transmembrane bacterial chemoreceptor. The Journal of Biological Chemistry 287:41697-41705. doi: 10.1074/jbc.M112.415588.
4. Armitage JP, Schmitt R. 1997. Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium melioti-variations on a theme? Microbiology 143:3671-3682. doi: 10.1099/00221287-143-12-3671.
5. Briegel A, Ames P, Gumbart J, Oikonomou CM, Parkinson JS, Jensen GJ. 2013. The mobility of two kinase domains in the Escherichia coli chemoreceptor array varies with signaling state. Molecular Microbiology 89:831-841. doi: 10.1111/mmi.12309.
6. Briegel A, Li X, Bilwes AM, Hughes KT, Jensen GJ, Crane BR. 2012. Bacterial chemoreceptor arrays are hexagonally packed trimers of receptor dimers networked by rings of kinase and coupling proteins. Proceedings of the National Academy of Sciences of the United States of America 109:3766-3771. doi: 10.1073/pnas.1115719109.
7. Briegel A, Ortega DR, Tocheva EI, Wuichet K, Li Z, Chen S, Müller A, Iancu CV, Murphy GE, Dobro MJ, Zhulin IB, Jensen GJ. 2009. Universal architecture of bacterial chemoreceptor arrays. Proceedings of the National Academy of Sciences of the United States of America 106:17181-17186. doi: 10.1073/pnas.0905181106.
8. Draheim RR, Bormans AF, Lai R-Z, Manson MD. 2006. Tuning a bacterial chemoreceptor with protein-membrane interactions. Biochemistry 45:14655-14664. doi: 10.1021/bi061259i.
9. Duke TAJ, Bray D. 1999. Heightened sensitivity of a lattice of membrane receptors. Proceedings of the National Academy of Sciences of the United States of America 96:10104-10108. doi: 10.1073/pnas.96.18.10104.
10. Ellis RJ. 2001. Macromolecular crowding: obvious but underappreciated. Trends in Biochemical Sciences 26:597-604. doi: 10.1016/S0968-0004(01)01938-7.
11. Endres RG, Wingreen NS. 2006. Precise adaptation in bacterial chemotaxis through "assistance neighborhoods". Proceedings of the National Academy of Sciences of the United States of America 103:13040-13044. doi: 10.1073/pnas.0603101103.
12. Englert DL, Adase CA, Jayaraman A, Manson MD. 2010. Repellent taxis in response to nickel ion reqires neither Ni2+ transport nor the periplasmic NikA binding protein. Journal of Bacteriology 192:2633-2637. doi: 10.1128/JB.00854-09.
13. Fowler DJ, Weis RM, Thompson LK. 2010. Kinase-active signaling complexes of bacterial chemoreceptors do not contain proposed receptor-receptor contacts observed in crystal structures. Biochemistry 49:1425-1434. doi: 10.1021/bi901565k.
14. Gan L, Jensen GJ. 2012. Electron tomography of cells. Quarterly Reviews of Biophysics 45:27-56. doi: 10.1017/S0033583511000102.
15. Gestwicki JE, Kiessling LL. 2002. Inter-receptor communication through arrays of bacterial chemoreceptors. Nature 415:81-84. doi: 10.1038/415081a.
16. Hazelbauer GL, Falke JJ, Parkinson JS. 2008. Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends in Biochemical Sciences 33:9-19. doi: 10.1016/j.tibs.2007.09.014.
17. Iancu CV, Tivol WF, Schooler JB, Dias DP, Henderson GP, Murphy GE, Wright ER, Li Z, Yu Z, Briegel A, Gan L, He Y, Jensen GJ. 2007. Electron cryotomography sample preparation using the Vitrobot. Nature Protocols 1:2813-2819. doi: 10.1038/nprot.2006.432.
18. Ind AC, Porter SL, Brown MT, Byles ED, de Beyer J, Godfrey SA, Armitage JP. 2009. An inducible expression plasmid for Rhodobacter sphaeroides and Paracoccus denitrificans. Applied and Environmental Biology 75:6613-6615. doi: 10.1128/AEM.01587-09.
19. Mudiyanselage AP, Yang M, Accomando LA, Thompson LK, Weis RM. 2013. Membrane Association of a protein increases rate, extent, and specificity of chemical cross-linking. Biochemistry 52:6127-6136. doi: 10.1021/bi4007176.
20. Kentner D, Sourjik V. 2006. Spatial organization of the bacterial chemotaxis system. Current Opinion in Microbiology 9:619-624. doi: 10.1016/j.mib.2006.10.012.
21. Kim KK, Yokota H, Kim SH. 1999. Four-helical-bundle structure of the cytoplasmic domain of a serine chemotaxis receptor. Nature 400:787-792. doi: 10.1038/23512.
22. Kleene SJ, Hobson AC, Adler J. 1979. Attractants and repellents influence methylation and demethylation of methyl-accepting chemotaxis proteins in an extract of Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 76:6309-6313. doi: 10.1073/pnas.76.12.6309.
23. Kremer JR, Mastronarde DN, McIntosh JR. 1996. Computer visualization of three-dimensional data using Imod. Journal of Structural Biology 116:71-76. doi: 10.1006/jsbi.1996.0013.
24. Ladinsky MS. 2010. Micromanipulator-assisted vitreous cryosectioning and sample preparation by high-pressure freezing. Methods in Enzymology 481:165-194. doi: 10.1016/S0076-6879(10)81008-0.
25. Ladinsky MS, Pierson JM, McIntosh JR. 2006. Vitreous cryo-sectioning of cells facilitated by a micromanipulator. Journal of Microscopy 224:129-134. doi: 10.1111/j.1365-2818.2006.01674.x.
26. Li G, Weis RM. 2000. Covalent modification regulates ligand binding to receptor complexes in the chemosensory system of Escherichia coli. Cell 100:357-365.
27. Li M, Hazelbauer GL. 2005. Adaptational assistance in clusters of bacterial chemoreceptors. Molecular Microbiology 56:1617-1626. doi: 10.1111/j.1365-2958.2005.04641.x.
28. Li X, Fleetwood AD, Bayas C, Bilwes AM, Ortega DR, Zhulin IB, Crane BR. 2013. The 3.2 Å resolution structure of a Receptor:CheA: CheW signaling complex defines overlapping binding sites and key residue interactions within bacterial chemosensory arrays. Biochemistry 52:3852-3865. doi: 10.1021/bi400383e.
29. Liu J, Hu B, Morado DR, Jani S, Manson MD, Margolin W. 2012. Molecular architecture of chemoreceptor arrays revealed by cryoelectron tomography of Escherichia coli minicells. Proceedings of the National Academy of Sciences of the United States of America 109:E1481-E1488. doi: 10.1073/pnas.1200781109.
30. Lupas A, Stock J. 1989. Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis. The Journal of Biological Chemistry 264:17337-17342.
31. Mastronarde DN. 2005. Automated electron microscope tomography using robust prediction of specimen movements. Journal of Structural Biology 152:36-51. doi: 10.1016/j.jsb.2005.07.007.
32. Milburn MV, Prive GG, Milligan DL, Scott WG, Yeh J, Jancarik J, Koshland DE Jnr, Kim SH. 1991. Three-dimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand. Science 254:1342-1347. doi: 10.1126/science.1660187.
33. Miller AS, Falke JJ. 2004. Side chains at the membrane-water interface modulate the signaling state of a transembrane receptor. Biochemistry 43:1763-1770. doi: 10.1021/bi0360206.
34. Montefusco DJ, Shrout AL, Besschetnova TY, Weis RM. 2007. Formation and activity of template-assembled receptor signaling complexes. Langmuir 23:3280-3289. doi: 10.1021/la062717r.
35. Natale AM, Duplantis JL, Piasta KN, Falke JJ. 2013. Structure, function, and on-off switching of a core unit contact between CheA kinase and CheW Adaptor protein in the bacterial chemosensory array: a disulfide mapping and mutagenesis study. Biochemisrty 52:7753-7765. doi: 10.1021/bi401159k.
36. Nicastro D, Schwartz CL, Pierson J, Gaudette R, Porter ME, McIntosh JR. 2006. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 313:944-948. doi: 10.1126/science.1128618.
37. Porter SL, Wadhams GH, Armitage JP. 2008. Rhodobacter sphaeroides: complexity in chemotactic signalling. Trends in Microbiology 16:251-260. doi: 10.1016/j.tim.2008.02.006.
38. Roberts MAJ, Wadhams GH, Hadfield KH, Tickner S., Armitage JP. 2012. ParA-like protein uses nonspecific chromosomal DNA binding to partition protein complexes. Proceedings of the National Academy of Sciences of the United States of America 109:6698-6703. doi: 10.1073/pnas.1114000109.
39. Shrout AL, Montefusco DJ, Weis RM. 2003. Template-directed assembly of receptor signalling complexes. Biochemistry 42:13379-13385. doi: 10.1021/bi0352769.
40. Silverman M, Simon MI. 1976. Operon controlling motility and chemotaxis in E. coli. Nature 264:577-580. doi: 10.1038/264577a0.
41. Sistrom WR. 1960. A requirement for sodium in the growth of Rhodopseudomonas sphaeroides. Journal of General Microbiology 22:778-785. doi: 10.1099/00221287-22-3-778.
42. Sourjik V, Berg H. 2002. Receptor sensitivity in bacterial chemotaxis. Proceedings of the National Academy of Sciences of the United States of America 99:123-127. doi: 10.1073/pnas.011589998.
43. Sourjik V, Berg HC. 2004. Functional interactions between receptors in bacterial chemotaxis. Nature 428:437-441. doi: 10.1038/nature02406.
44. Studdert CA, Parkinson JS. 2004. Crosslinking snapshots of bacterial chemoreceptor squads. Proceedings of the National Academy of Sciences of the United States of America 101:2117-2122. doi: 10.1073/pnas.0308622100.
45. Swulius MT, Jensen GJ. 2012. The helical MreB cytoskeleton in E. coli MC1000/pLE7 is an artifact of the N-terminal YFP tag. Journal of Bacteriology 194:6382-6386. doi: 10.1128/JB.00505-12.
46. Tam R, Saier MHJ. 1993. Structural, functional, and evolutionary relationships among extracellular solute-binding receptors of bacteria. Microbiological Reviews 57:320-346.
47. Thompson SR, Wadhams GH, Armitage JP. 2006. The positioning of cytolasmic protein clusters in bacteria. Proceedings of the National Academy of Sciences of the United States of America 103:8209-8214. doi: 10.1073/pnas.0600919103.
48. Tivol W, Briegel A, Jensen GJ. 2008. An improved cryogen for plunge freezing. Microscopy and Microanalysis 14:375-379. doi: 10.1017/S1431927608080781.
49. Toews ML, Goy MF, Springer MS, Adler J. 1979. Attractants and repellents control demethylation of methylated chemotaxis proteins in Escherichia coli. Proceedings of the National Academy of Sciences of the United States of America 76:5544-5548. doi: 10.1073/pnas.76.11.5544.
50. Turner L, Ryu WS, Berg HC. 2000. Real-time imaging of fluorescent flagellar filaments. Journal of Bacteriology 182:2793-2801. doi: 10.1128/JB.182.10.2793-2801.2000.
51. Ulrich LE, Zhulin IB. 2010. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Research 38:D401-D407. doi: 10.1093/nar/gkp940.
52. Wadhams GH, Armitage JP. 2004. Making sense of it all: bacterial chemotaxis. Nature Reviews Molecular Cell Biology 5:1024-1037. doi: 10.1038/nrm1524.
53. Wadhams GH, Martin AC, Porter SL, Maddock JR, Mantotta JC, King HM, Armitage JP. 2002. TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Molecular Microbiology 46:1211-1221. doi: 10.1046/j.1365-2958.2002.03252.x.
54. Wadhams GH, Warren AV, Martin AC, Armitage JP. 2003. Targeting of two signal transduction pathways to different regions of the bacterial cell. Molecular Microbiology 50:763-770. doi: 10.1046/j.1365-2958.2003.03716.x.
55. Wuichet K, Zhulin IB. 2010. Origins and diversification of a complex signal transduction system in prokaryotes. Science Sinaling 3:ra50. doi: 10.1126/scisignal.2000724.
56. Zheng QS, Keszthelyi B, Branlund E, Lyle JM, Braunfeld MB, Sedat JW, Agard DA. 2007. UCSF tomography: an integrated software suite for real-time electron microscopic tomographic data collection, alignment and reconstruction. Journal of Structural Biology 157:138-147. doi: 10.1016/j.jsb.2006.06.005.
57. Zhou H-X. 2013. Influence of crowded cellular environments on protein folding, binding, and oligomerization: biological consequences and potentials of atomistic modeling. FEBS Letters 587:1053-1061. doi: 10.1016/j.febslet.2013.01.064.
58. Zhou H-X, Rivas G, Minton AP. 2008. Macromolecular crowding and confinement: biochemical, biophysical, and potential physiological consequences. Annual Review of Biophysics 37:375-397. doi: 10.1146/annurev.biophys.37.032807.125817.