CheR- and CheB-Dependent Chemosensory Adaptation System of Rhodobacter sphaeroides
10.1128/jb.183.24.7135-7144.2001
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

ABSTRACT Rhodobacter sphaeroides has multiple homologues of most of the Escherichia coli chemotaxis genes, organized in three major operons and other, unlinked, loci. These include cheA 1 and cheR 1 ( che Op 1 ) and cheA 2 , cheR 2 , and cheB 1 ( che Op 2 ). In-frame deletions of these cheR and cheB homologues were constructed and the chemosensory behaviour of the resultant mutants examined on swarm plates and in tethered cell assays. Under the conditions tested, CheR 2 and CheB 1 were essential for normal chemotaxis, whereas CheR 1 was not. cheR 2 and cheB 1 , but not cheR 1 , were also able to complement the equivalent E. coli mutants. However, none of the proteins were required for the correct polar localization of the chemoreceptor McpG in R. sphaeroides . In E. coli, CheR binds to the NWETF motif on the high-abundance receptors, allowing methylation of both high- and low-abundance receptors. This motif is not contained on any R. sphaeroides chemoreceptors thus far identified, although 2 of the 13 putative chemoreceptors, McpA and TlpT, do have similar sequences. This suggests that CheR 2 either interacts with the NWETF motif of E. coli methyl-accepting chemotaxis proteins (MCPs), even though its native motif may be slightly different, or with another conserved region of the MCPs. Methanol release measurements show that R. sphaeroides has an adaptation system that is different from that of Bacillus subtilis and E. coli, with methanol release measurable on the addition of attractant but not on its removal. Intriguingly, CheA 2 , but not CheA 1 , is able to phosphorylate CheB 1 , suggesting that signaling through CheA 1 cannot initiate feedback receptor adaptation via CheB 1 -P.

Bibliography

Martin, A. C., Wadhams, G. H., Shah, D. S. H., Porter, S. L., Mantotta, J. C., Craig, T. J., Verdult, P. H., Jones, H., & Armitage, J. P. (2001). CheR- and CheB-Dependent Chemosensory Adaptation System of Rhodobacter sphaeroides. Journal of Bacteriology, 183(24), 7135–7144.

Authors 9
  1. Angela C. Martin (first)
  2. George H. Wadhams (additional)
  3. Deepan S. H. Shah (additional)
  4. Steven L. Porter (additional)
  5. Jeevani C. Mantotta (additional)
  6. Tim J. Craig (additional)
  7. Peter H. Verdult (additional)
  8. Helen Jones (additional)
  9. Judith P. Armitage (additional)
References 54 Referenced 35
  1. Alam M. Lebert M. Oesterhelt D. Hazelbauer G. L. Methyl-accepting taxis proteins in Halobacterium halobium.EMBO J.81989631639 (10.1002/j.1460-2075.1989.tb03418.x) / EMBO J. / Methyl-accepting taxis proteins in Halobacterium halobium by Alam M. (1989)
  2. Armitage J. P. Bacterial tactic responses.Adv. Microb. Physiol.411999229289 (10.1016/S0065-2911(08)60168-X) / Adv. Microb. Physiol. / Bacterial tactic responses by Armitage J. P. (1999)
  3. 10.1128/jb.169.2.514-518.1987
  4. Armitage J. P. Schmitt R. Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti—variations on a theme? Microbiology 143 1997 3671 3682 (10.1099/00221287-143-12-3671) / Microbiology / Bacterial chemotaxis: Rhodobacter sphaeroides and Sinorhizobium meliloti—variations on a theme? by Armitage J. P. (1997)
  5. Borkovich K. A. Alex L. A. Simon M. I. Attenuation of sensory receptor signaling by covalent modification.Proc. Natl. Acad. Sci. USA89199267566760 (10.1073/pnas.89.15.6756) / Proc. Natl. Acad. Sci. USA / Attenuation of sensory receptor signaling by covalent modification by Borkovich K. A. (1992)
  6. Borkovich K. A. Kaplan N. Hess J. F. Simon M. I. Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer.Proc. Natl. Acad. Sci. USA86198912081212 (10.1073/pnas.86.4.1208) / Proc. Natl. Acad. Sci. USA / Transmembrane signal transduction in bacterial chemotaxis involves ligand-dependent activation of phosphate group transfer by Borkovich K. A. (1989)
  7. Borkovich K. A. Simon M. I. The dynamics of protein phosphorylation in bacterial chemotaxis.Cell63199013391348 (10.1016/0092-8674(90)90429-I) / Cell / The dynamics of protein phosphorylation in bacterial chemotaxis by Borkovich K. A. (1990)
  8. 10.1128/JB.182.24.6865-6873.2000
  9. Djordjevic S. Stock A. M. Structural analysis of bacterial chemotaxis proteins: components of a dynamic signaling system.J. Struct. Biol.1241998189200 (10.1006/jsbi.1998.4034) / J. Struct. Biol. / Structural analysis of bacterial chemotaxis proteins: components of a dynamic signaling system by Djordjevic S. (1998)
  10. Falke J. J. Bass R. B. Butler S. L. Chervitz S. A. Danielson M. A. 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.131997457512 (10.1146/annurev.cellbio.13.1.457) / Annu. Rev. Cell Dev. Biol. / The two-component signaling pathway of bacterial chemotaxis: a molecular view of signal transduction by receptors, kinases, and adaptation enzymes by Falke J. J. (1997)
  11. 10.1128/jb.179.21.6714-6720.1997
  12. 10.1128/JB.181.10.3164-3171.1999
  13. Hamblin P. A. Maguire B. A. Grishanin R. N. Armitage J. P. Evidence for two chemosensory pathways in Rhodobacter sphaeroides.Mol. Microbiol.26199710831096 (10.1046/j.1365-2958.1997.6502022.x) / Mol. Microbiol. / Evidence for two chemosensory pathways in Rhodobacter sphaeroides by Hamblin P. A. (1997)
  14. Harrison D. M. Skidmore J. Armitage J. P. Maddock J. R. Localization and environmental regulation of MCP-like proteins in Rhodobacter sphaeroides.Mol. Microbiol.311999885892 (10.1046/j.1365-2958.1999.01226.x) / Mol. Microbiol. / Localization and environmental regulation of MCP-like proteins in Rhodobacter sphaeroides by Harrison D. M. (1999)
  15. Hess J. F. Oosawa K. Kaplan N. Simon M. I. Phosphorylation of three proteins in the signalling pathway of bacterial chemotaxis.Cell5319887987 (10.1016/0092-8674(88)90489-8) / Cell / Phosphorylation of three proteins in the signalling pathway of bacterial chemotaxis by Hess J. F. (1988)
  16. Jeziore-Sassoon Y. Hamblin P. A. Bootle W. C. Poole P. S. Armitage J. P. Metabolism is required for chemotaxis to sugars in Rhodobacter sphaeroides.Microbiology1441998229239 (10.1099/00221287-144-1-229) / Microbiology / Metabolism is required for chemotaxis to sugars in Rhodobacter sphaeroides by Jeziore-Sassoon Y. (1998)
  17. Jurica M. S. Stoddard B. L. Mind your B's and R's: bacterial chemotaxis, signal transduction and protein recognition.Structure61998809813 (10.1016/S0969-2126(98)00082-3) / Structure / Mind your B's and R's: bacterial chemotaxis, signal transduction and protein recognition by Jurica M. S. (1998)
  18. Kehry M. R. Doak T. G. Dahlquist F. W. Stimulus-induced changes in methylesterase activity during chemotaxis in Escherichia coli.J. Biol. Chem.25919841182811835 (10.1016/S0021-9258(20)71286-X) / J. Biol. Chem. / Stimulus-induced changes in methylesterase activity during chemotaxis in Escherichia coli by Kehry M. R. (1984)
  19. Kirby J. R. Kristich C. J. Feinberg S. L. Ordal G. W. Methanol production during chemotaxis to amino acids in Bacillus subtilis.Mol. Microbiol.241997869878 (10.1046/j.1365-2958.1997.3941759.x) / Mol. Microbiol. / Methanol production during chemotaxis to amino acids in Bacillus subtilis by Kirby J. R. (1997)
  20. Kirby J. R. Saulmon M. M. Kristich C. J. Ordal G. W. CheY-dependent methylation of the asparagine receptor, McpB, during chemotaxis in Bacillus subtilis.J. Biol. Chem.27419991109211100 (10.1074/jbc.274.16.11092) / J. Biol. Chem. / CheY-dependent methylation of the asparagine receptor, McpB, during chemotaxis in Bacillus subtilis by Kirby J. R. (1999)
  21. 10.1128/JB.182.11.3017-3021.2000
  22. 10.1038/227680a0
  23. Lupas A. Stock J. Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis.J. Biol. Chem.26419891733717342 (10.1016/S0021-9258(18)71497-X) / J. Biol. Chem. / Phosphorylation of an N-terminal regulatory domain activates the CheB methylesterase in bacterial chemotaxis by Lupas A. (1989)
  24. 10.1128/JB.181.17.5527-5529.1999
  25. 10.1126/science.8456299
  26. Martin A. C. Wadhams G. H. Armitage J. P. The roles of the multiple CheW and CheA homologues in chemotaxis and in chemoreceptor localization in Rhodobacter sphaeroides.Mol. Microbiol.40200112611272 (10.1046/j.1365-2958.2001.02468.x) / Mol. Microbiol. / The roles of the multiple CheW and CheA homologues in chemotaxis and in chemoreceptor localization in Rhodobacter sphaeroides by Martin A. C. (2001)
  27. 10.1128/jb.175.1.133-140.1993
  28. Mowbray S. L. Sandgren M. O. Chemotaxis receptors: a progress report on structure and function.J. Struct. Biol.1241998257275 (10.1006/jsbi.1998.4043) / J. Struct. Biol. / Chemotaxis receptors: a progress report on structure and function by Mowbray S. L. (1998)
  29. Ninfa E. G. Stock A. Mowbray S. Stock J. Reconstruction of the bacterial chemotaxis signal transduction system from purified components.J. Biol. Chem.266199197649770 (10.1016/S0021-9258(18)92886-3) / J. Biol. Chem. / Reconstruction of the bacterial chemotaxis signal transduction system from purified components by Ninfa E. G. (1991)
  30. Nordmann B. Lebert M. R. Alam M. Nitz S. Kollmannsberger H. Oesterhelt D. Hazelbauer G. L. Identification of volatile forms of methyl groups released by Halobacterium salinarium.J. Biol. Chem.26919941644916454 (10.1016/S0021-9258(17)34027-9) / J. Biol. Chem. / Identification of volatile forms of methyl groups released by Halobacterium salinarium by Nordmann B. (1994)
  31. Penfold R. J. Pemberton J. M. An improved suicide vector for construction of chromosomal insertion mutations in bacteria.Gene1181992145146 (10.1016/0378-1119(92)90263-O) / Gene / An improved suicide vector for construction of chromosomal insertion mutations in bacteria by Penfold R. J. (1992)
  32. 10.1128/jb.170.12.5673-5679.1988
  33. Rosario M. M. Kirby J. R. Bochar D. A. Ordal G. W. Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD.Biochemistry34199538233831 (10.1021/bi00011a040) / Biochemistry / Chemotactic methylation and behavior in Bacillus subtilis: role of two unique proteins, CheC and CheD by Rosario M. M. (1995)
  34. Rosario M. M. Ordal G. W. CheC and CheD interact to regulate methylation of Bacillus subtilis methyl-accepting chemotaxis proteins.Mol. Microbiol.211996511518 (10.1111/j.1365-2958.1996.tb02560.x) / Mol. Microbiol. / CheC and CheD interact to regulate methylation of Bacillus subtilis methyl-accepting chemotaxis proteins by Rosario M. M. (1996)
  35. Sambrook J. Fritsch E. F. Maniatis T. Molecular cloning: a laboratory manual 2nd ed. 1989 Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y
  36. Schafer A. Tauch A. Jager W. Kalinowski J. Thierbach G. Puhler A. Small mobilizable multipurpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum.Gene14519946973 (10.1016/0378-1119(94)90324-7) / Gene / Small mobilizable multipurpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum by Schafer A. (1994)
  37. Shah D. S. Porter S. L. Harris D. C. Wadhams G. H. Hamblin P. A. Armitage J. P. Identification of a fourth cheY gene in Rhodobacter sphaeroides and interspecies interaction within the bacterial chemotaxis signal transduction pathway.Mol. Microbiol.352000101112 (10.1046/j.1365-2958.2000.01680.x) / Mol. Microbiol. / Identification of a fourth cheY gene in Rhodobacter sphaeroides and interspecies interaction within the bacterial chemotaxis signal transduction pathway by Shah D. S. (2000)
  38. Shiomi D. Okumura H. Homma M. Kawagishi I. The aspartate chemoreceptor Tar is effectively methylated by binding to the methyltransferase mainly through hydrophobic interaction.Mol. Microbiol.362000132140 (10.1046/j.1365-2958.2000.01834.x) / Mol. Microbiol. / The aspartate chemoreceptor Tar is effectively methylated by binding to the methyltransferase mainly through hydrophobic interaction by Shiomi D. (2000)
  39. Sistrom W. R. A requirement for sodium in the growth of Rhodopseudomonas sphaeroides.J. Gen. Microbiol.221960778785 (10.1099/00221287-22-3-778) / J. Gen. Microbiol. / A requirement for sodium in the growth of Rhodopseudomonas sphaeroides by Sistrom W. R. (1960)
  40. 10.1128/JB.182.4.967-973.2000
  41. Sockett R. E. Foster J. C. A. Armitage J. P. Molecular biology of the Rhodobacter sphaeroides flagellum.FEMS Symp.531990473479 / FEMS Symp. / Molecular biology of the Rhodobacter sphaeroides flagellum by Sockett R. E. (1990)
  42. Springer W. R. Koshland D. E. Jr. Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system.Proc. Natl. Acad. Sci. USA741977533537 (10.1073/pnas.74.2.533) / Proc. Natl. Acad. Sci. USA / Identification of a protein methyltransferase as the cheR gene product in the bacterial sensing system by Springer W. R. (1977)
  43. Spudich E. N. Takahashi T. Spudich J. L. Sensory rhodopsin I and II modulate a methylation/demethylation system in Halobacterium halobium.Proc. Natl. Acad. Sci. USA86198977467750 (10.1073/pnas.86.20.7746) / Proc. Natl. Acad. Sci. USA / Sensory rhodopsin I and II modulate a methylation/demethylation system in Halobacterium halobium by Spudich E. N. (1989)
  44. Stock J. B. Clarke S. Koshland D. E. Jr. The protein carboxymethyltransferase involved in Escherichia coli and Salmonella typhimurium chemotaxis.Meth. Enzymol.1061984310321 (10.1016/0076-6879(84)06031-6) / Meth. Enzymol. / The protein carboxymethyltransferase involved in Escherichia coli and Salmonella typhimurium chemotaxis by Stock J. B. (1984)
  45. Stock J. B. Maderis A. M. Koshland D. E. Jr. Bacterial chemotaxis in the absence of receptor carboxyl methylation.Cell2719813744 (10.1016/0092-8674(81)90358-5) / Cell / Bacterial chemotaxis in the absence of receptor carboxyl methylation by Stock J. B. (1981)
  46. Stock J. B. Surette M. G. Chemotaxis Escherichia coli and Salmonella: cellular and molecular biology 2nd ed. Neidhardt F. C. Curtiss R. III Ingraham J. L. Lin E. C. C. Low K. B. Magasanik B. Reznikoff W. S. Riley M. Schaechter M. Umbarger H. E. 1996 1103 1129 ASM Press Washington D.C.
  47. Thoelke M. S. Kirby J. R. Ordal G. W. Novel methyl transfer during chemotaxis in Bacillus subtilis.Biochemistry28198955855589 (10.1021/bi00439a037) / Biochemistry / Novel methyl transfer during chemotaxis in Bacillus subtilis by Thoelke M. S. (1989)
  48. Wadhams G. H. Martin A. C. Armitage J. P. Identification and localization of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides.Mol. Microbiol.36200012221233 (10.1046/j.1365-2958.2000.01936.x) / Mol. Microbiol. / Identification and localization of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides by Wadhams G. H. (2000)
  49. Ward M. J. Bell A. W. Hamblin P. A. Packer H. L. Armitage J. P. Identification of a chemotaxis operon with 2 cheY genes in Rhodobacter sphaeroides.Mol. Microbiol.171995357366 (10.1111/j.1365-2958.1995.mmi_17020357.x) / Mol. Microbiol. / Identification of a chemotaxis operon with 2 cheY genes in Rhodobacter sphaeroides by Ward M. J. (1995)
  50. Ward M. J. Harrison D. M. Ebner M. J. Armitage J. P. Identification of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides.Mol. Microbiol.181995115121 (10.1111/j.1365-2958.1995.mmi_18010115.x) / Mol. Microbiol. / Identification of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides by Ward M. J. (1995)
  51. 10.1128/JB.180.4.914-920.1998
  52. 10.1128/jb.169.5.1878-1885.1987
  53. Wu J. G. Li J. Y. Li G. Y. Long D. G. Weis R. M. The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation.Biochemistry35199649844993 (10.1021/bi9530189) / Biochemistry / The receptor binding site for the methyltransferase of bacterial chemotaxis is distinct from the sites of methylation by Wu J. G. (1996)
  54. 10.1128/jb.156.3.1228-1235.1983
Dates
Type When
Created 23 years, 1 month ago (July 27, 2002, 6:01 a.m.)
Deposited 4 years ago (July 29, 2021, 2:01 p.m.)
Indexed 1 year, 2 months ago (June 21, 2024, 4:28 a.m.)
Issued 23 years, 8 months ago (Dec. 15, 2001)
Published 23 years, 8 months ago (Dec. 15, 2001)
Published Print 23 years, 8 months ago (Dec. 15, 2001)
Funders 0

None

@article{Martin_2001, title={CheR- and CheB-Dependent Chemosensory Adaptation System of Rhodobacter sphaeroides}, volume={183}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.183.24.7135-7144.2001}, DOI={10.1128/jb.183.24.7135-7144.2001}, number={24}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Martin, Angela C. and Wadhams, George H. and Shah, Deepan S. H. and Porter, Steven L. and Mantotta, Jeevani C. and Craig, Tim J. and Verdult, Peter H. and Jones, Helen and Armitage, Judith P.}, year={2001}, month=dec, pages={7135–7144} }