DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment
10.1128/jb.176.2.344-350.1994
Crossref journal-article
American Society for Microbiology
Journal of Bacteriology (235)
Abstract

The amino acid sequence of DcrA from Desulfovibrio vulgaris Hildenborough, a strictly anaerobic, sulfate-reducing bacterium, indicated homology with the methyl-accepting chemotaxis proteins from enteric bacteria (A. Dolla, R. Fu, M. J. Brumlik, and G. Voordouw, J. Bacteriol. 174:1726-1733, 1992). The homology is restricted to the cytoplasmic C-terminal signaling domain. The periplasmic N-terminal sensor domain was found to contain a unique sequence, CHHCH, corresponding to a consensus c-type heme binding site. A pretreated, DcrA-specific polyclonal antiserum, generated against DcrA protein overproduced in Escherichia coli, was used for immunoprecipitation of 35S-labeled DcrA from D. vulgaris and Desulfovibrio desulfuricans G200(pJRFR2), a transconjugant that overexpresses functional DcrA. Labeling of the latter with the heme precursor 5-amino-[4-14C]levulinic acid, followed by immunoprecipitation, sodium dodecyl sulfate-polyacrylamide gel electrophoresis, and fluorography, confirmed the presence of c-type heme, while labeling with L-[methyl-3H]methionine in the absence of protein synthesis confirmed that DcrA is a methyl-accepting protein. The base liability of the incorporated radioactivity indicated methyl ester formation like that occurring in the methyl-accepting chemotaxis proteins of enteric bacteria. L-[methyl-3H]methionine labeling of D. desulfuricans G200(pJRFR2) under different conditions indicated that methyl labeling of DcrA decreased upon addition of oxygen and increased upon subsequent addition of the reducing agent dithionite. These results indicate that DcrA may serve as a sensor of oxygen concentration and/or redox potential.

Bibliography

Fu, R., Wall, J. D., & Voordouw, G. (1994). DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment. Journal of Bacteriology, 176(2), 344–350.

Authors 3
  1. R Fu (first)
  2. J D Wall (additional)
  3. G Voordouw (additional)
References 43 Referenced 70
  1. Alam , M. , M. Lebert , D. Oesterhelt , and G. L. Hazelbauer . 1989 . Methyl-accepting taxis proteins in Halobacterium halobium . EMBO J. 8 : 631 - 639 . (10.1002/j.1460-2075.1989.tb03418.x) / EMBO J. / Methyl-accepting taxis proteins in Halobacterium halobium by Alam M. (1989)
  2. Ames , P. , and J. S. Parkinson . 1988 . Transmembrane signaling by bacterial chemoreceptors: E. coli transducers with locked signal output . Cell 55 : 817 - 826 . (10.1016/0092-8674(88)90137-7) / Cell / Transmembrane signaling by bacterial chemoreceptors: E. coli transducers with locked signal output by Ames P. (1988)
  3. Borkovich , K. A. , and M. I. Simon . 1990 . The dynamics of protein phosphorylation in bacterial chemotaxis . Cell 63 : 1339 - 1348 . (10.1016/0092-8674(90)90429-I) / Cell / The dynamics of protein phosphorylation in bacterial chemotaxis by Borkovich K. A. (1990)
  4. Bruschi , M. , P. Bertrand , C. More , G. Leroy , J. Bonicel , J. Haladjian , G. Chottard , W. B. R. Pollock , and G. Voordouw . 1992 . Biochemical and spectroscopic characterization of the high molecular weight cytochrome c from Desulfovibrio vulgaris Hildenborough expressed in Desulfovibrio desulfuricans G200 . Biochemistry 31 : 3281 - 3288 . (10.1021/bi00127a033) / Biochemistry / Biochemical and spectroscopic characterization of the high molecular weight cytochrome c from Desulfovibrio vulgaris Hildenborough expressed in Desulfovibrio desulfuricans G200 by Bruschi M. (1992)
  5. Chelsky , D. , N. I. Gutterson , and D. E. Koshland , Jr. 1984 . A diffusion assay for detection and quantitation of methyl-esterified proteins on polyacrylamide gels . Anal. Biochem. 141 : 143 - 148 . (10.1016/0003-2697(84)90437-8) / Anal. Biochem. / A diffusion assay for detection and quantitation of methyl-esterified proteins on polyacrylamide gels by Chelsky D. (1984)
  6. Davison , J. , M. Heusterpreute , N. Chevalier , H. T. Vinh , and F. Brunel . 1987 . Vectors with restriction site banks. V. pJRD215, a wide-host range cosmid vector with multiple cloning sites . Gene 51 : 275 - 280 . (10.1016/0378-1119(87)90316-7) / Gene / Vectors with restriction site banks. V. pJRD215, a wide-host range cosmid vector with multiple cloning sites by Davison J. (1987)
  7. Deckers , H. M. , and G. Voordouw . 1994 . Identification of a large family of genes for putative chemoreceptor proteins in an ordered library of the Desulfovibrio vulgaris Hildenborough genome . J. Bacteriol. 176 : 351 - 358 . (10.1128/jb.176.2.351-358.1994) / J. Bacteriol. / Identification of a large family of genes for putative chemoreceptor proteins in an ordered library of the Desulfovibrio vulgaris Hildenborough genome by Deckers H. M. (1994)
  8. Deckers , H. M. , and G. Voordouw . 1994 . Membrane topology of the methyl-accepting chemotaxis protein DcrA from Desulfovibrio vulgaris Hildenborough . Antonie Leeuwenhoek 65 : 1 - 6 . (10.1007/BF00878273) / Antonie Leeuwenhoek / Membrane topology of the methyl-accepting chemotaxis protein DcrA from Desulfovibrio vulgaris Hildenborough by Deckers H. M. (1994)
  9. .Deckers H. M. and G. Voordouw. Unpublished data.
  10. DeFranco , A. L. , and D. E. Koshland , Jr. 1980 . Multiple methylation in processing of sensory signals during bacterial chemotaxis . Proc. Natl. Acad. Sci. USA 77 : 2429 - 2433 . (10.1073/pnas.77.5.2429) / Proc. Natl. Acad. Sci. USA / Multiple methylation in processing of sensory signals during bacterial chemotaxis by DeFranco A. L. (1980)
  11. Dolla , A. , R. Fu , M. J. Brumlik , and G. Voordouw . 1992 . Nucleotide sequence of dcrA, a Desulfovibrio vulgaris Hildenborough chemoreceptor gene, and its expression in Escherichia coli . J. Bacteriol. 174 : 1726 - 1733 . (10.1128/jb.174.6.1726-1733.1992) / J. Bacteriol. / Nucleotide sequence of dcrA, a Desulfovibrio vulgaris Hildenborough chemoreceptor gene, and its expression in Escherichia coli by Dolla A. (1992)
  12. Engelmann , T. W. 1881 . Neue Methode zur Untersuchung der Sauerstoffausscheidung planzlicher und tierischer Organismen . Pfluegers Arch. Gesamte Physiol. Menschen Tiere 25 : 285 - 292 . (10.1007/BF01661982) / Pfluegers Arch. Gesamte Physiol. Menschen Tiere / Neue Methode zur Untersuchung der Sauerstoffausscheidung planzlicher und tierischer Organismen by Engelmann T. W. (1881)
  13. Engstrom , P. , and G. L. Hazelbauer . 1980 . Multiple methylation of methyl-accepting chemotaxis proteins during adaptation of E. coli chemical stimuli . Cell 20 : 165 - 171 . (10.1016/0092-8674(80)90244-5) / Cell / Multiple methylation of methyl-accepting chemotaxis proteins during adaptation of E. coli chemical stimuli by Engstrom P. (1980)
  14. Finzel , B. C. , P. C. Weber , K. D. Hardman , and F. R. Salemme . 1985 . Structure of ferricytochrome c' from Rhodospirillum molischianum at 1.67 A resolution . J. Mol. Biol. 186 : 627 - 643 . (10.1016/0022-2836(85)90135-4) / J. Mol. Biol. / Structure of ferricytochrome c' from Rhodospirillum molischianum at 1.67 A resolution by Finzel B. C. (1985)
  15. Fu R. and G. Voordouw. 1993. A methyl-accepting chemotaxis protein from Desulfovibrio vulgaris Hildenborough contains a c-type heme and functions as an oxygen sensor abstr. 1-72. Abstr. 93rd Gen. Meet. Am. Soc. Microbiol. 1993. American Society for Microbiology Washington D.C.
  16. Hamilton , W. A. 1985 . Sulphate-reducing bacteria and anaerobic corrosion. Annu . Rev. Microbiol. 39 : 195 - 217 . (10.1146/annurev.mi.39.100185.001211) / Rev. Microbiol. / Sulphate-reducing bacteria and anaerobic corrosion. Annu by Hamilton W. A. (1985)
  17. Hanahan D. 1985. Techniques for transformation of E. coli p. 109-136. In D. M. Glover (ed.) DNA cloning vol. I. IRL Press Washington D.C.
  18. Harwood , C. S. 1989 . A methyl-accepting protein is involved in benzoate taxis in Pseudomonasputida . J. Bacteriol. 171 : 4603 - 4608 . (10.1128/jb.171.9.4603-4608.1989) / J. Bacteriol. / A methyl-accepting protein is involved in benzoate taxis in Pseudomonasputida by Harwood C. S. (1989)
  19. Hederstedt , L. , and C. von Wachenfeldt . 1990 . Bacillus subtilis 13-kilodalton cytochrome c-550 encoded by cccA consists of a membrane-anchor and a heme domain . J. Biol. Chem. 265 : 13939 - 13948 . (10.1016/S0021-9258(18)77439-5) / J. Biol. Chem. / Bacillus subtilis 13-kilodalton cytochrome c-550 encoded by cccA consists of a membrane-anchor and a heme domain by Hederstedt L. (1990)
  20. Macnab R. M. 1987. Motility and chemotaxis p. 732-759. In F. C. Neidhardt J. L. Ingraham K. B. Low B. Magasanik M. Schaechter and H. E. Umbarger (ed.) Escherichia coli and Salmonella typhimurium: cellular and molecular biology vol. 1. American Society for Microbiology Washington D.C.
  21. Milburn , M. V. , G. G. Prive , D. L. Milligan , W. G. Scott , J. Yeh , J. Jancarik , D. E. Koshland , Jr. , and S.-H. Kim . 1992 . Threedimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand . Science 254 : 1342 - 1347 . (10.1126/science.1660187) / Science / Threedimensional structures of the ligand-binding domain of the bacterial aspartate receptor with and without a ligand by Milburn M. V. (1992)
  22. Moore G. R. and G. W. Pettigrew. 1990. Springer series in molecular biology. Cytochromes c: evolutionary structural and physicochemical aspects p. 150-151 and 230-239. Springer-Verlag New York.
  23. Parkinson , J. S. 1993 . Signal transduction schemes in bacteria . Cell 73 : 857 - 871 . (10.1016/0092-8674(93)90267-T) / Cell / Signal transduction schemes in bacteria by Parkinson J. S. (1993)
  24. Pfennig N. F. Widdel and H. G. Truper. 1981. The dissimilatory sulphate-reducing bacteria p. 926-940. In M. P. Starr H. Stolp H. Triiper A. Balows and H. G. Schlegel (ed.) The prokaryotes: a handbook on habitats isolation and identification of bacteria vol. I. Springer-Verlag New York. (10.1007/978-3-662-13187-9_74)
  25. Pollock , W. B. R. , M. Loutfi , M. Bruschi , B. J. Rapp-Giles , J. D. Wall , and G. Voordouw . 1991 . Cloning, sequencing, and expression of the gene encoding the high-molecular-weight cytochrome c from Desulfovibrio vulgaris Hildenborough . J. Bacteriol. 173 : 220 - 228 . (10.1128/JB.173.1.220-228.1991) / J. Bacteriol. / Cloning, sequencing, and expression of the gene encoding the high-molecular-weight cytochrome c from Desulfovibrio vulgaris Hildenborough by Pollock W. B. R. (1991)
  26. Postgate J. R. 1984. The sulphate-reducing bacteria 2nd ed. p. 32-33. Cambridge University Press Cambridge.
  27. Rossi , M. , W. B. R. Pollock , M. W. Rei J , R. G. Keon , R. Fu , and G. Voordouw . 1993 . The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex . J. Bacteriol. 175 : 4699 - 4711 . (10.1128/JB.175.15.4699-4711.1993) / J. Bacteriol. / The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex by Rossi M. (1993)
  28. Sambrook J. E. F. Fritsch and T. Maniatis. 1989. Molecular cloning: a laboratory manual 2nd ed. p. 18.44-18.46. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
  29. Shioi , J. , R. C. Tribhuwan , S. T. Berg , and B. L. Taylor . 1988 . Signal transduction in chemotaxis to oxygen in Escherichia coli and Salmonella typhimurium . J. Bacteriol. 170 : 5507 - 5511 . (10.1128/jb.170.12.5507-5511.1988) / J. Bacteriol. / Signal transduction in chemotaxis to oxygen in Escherichia coli and Salmonella typhimurium by Shioi J. (1988)
  30. Springer , M. S. , M. F. Goy , and J. Adler . 1977 . Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins . Proc. Natl. Acad. Sci. USA 74 : 3312 - 3316 . (10.1073/pnas.74.8.3312) / Proc. Natl. Acad. Sci. USA / Sensory transduction in Escherichia coli: two complementary pathways of information processing that involve methylated proteins by Springer M. S. (1977)
  31. Springer , M. S. , M. F. Goy , and J. Adler . 1979 . Protein methylation in behavioral control mechanisms and in signal transduction . Nature (London) 280 : 279 - 284 . (10.1038/280279a0) / Nature (London) / Protein methylation in behavioral control mechanisms and in signal transduction by Springer M. S. (1979)
  32. Stock , J. B. , G. S. Lukat , and A. M. Stock . 1991 . Bacterial chemotaxis and the molecular logic of intracellular signal transduction networks. Annu . Rev. Biophys. Biophys. Chem. 20 : 109 - 136 . (10.1146/annurev.bb.20.060191.000545) / Rev. Biophys. Biophys. Chem. / Bacterial chemotaxis and the molecular logic of intracellular signal transduction networks. Annu by Stock J. B. (1991)
  33. Tabor S. 1990. Expression using the T7 RNA polymerase/promoter system p. 16.2.1-16.2.11. In F. M. Ausubel et al. (ed.) Current protocols in molecular biology. Greene Publishing Associates and Wiley Interscience New York. (10.1002/0471142727.mb1602s11)
  34. Taylor , B. L. 1983 . Role of proton motive force in sensory transduction in bacteria. Annu . Rev. Microbiol. 37 : 551 - 573 . (10.1146/annurev.mi.37.100183.003003) / Rev. Microbiol. / Role of proton motive force in sensory transduction in bacteria. Annu by Taylor B. L. (1983)
  35. van den Berg , W. A. M. , W. M. A. M. van Dongen , and C. Veeger . 1991 . Reduction of the amount of periplasmic hydrogenase in Desulfovibrio vulgaris (Hildenborough) with antisense RNA: direct evidence for an important role of this hydrogenase in lactate metabolism . J. Bacteriol. 173 : 3688 - 3694 . (10.1128/JB.173.12.3688-3694.1991) / J. Bacteriol. / Reduction of the amount of periplasmic hydrogenase in Desulfovibrio vulgaris (Hildenborough) with antisense RNA: direct evidence for an important role of this hydrogenase in lactate metabolism by van den Berg W. A. M. (1991)
  36. Van Rooqen , G. J. H. , M. Bruschi , and G. Voordouw . 1989 . Cloning and sequencing of the gene encoding cytochrome C553 from Desulfovibrio vulgaris Hildenborough . J. Bacteriol. 171 : 3575 - 3578 . (10.1128/jb.171.6.3575-3578.1989) / J. Bacteriol. / Cloning and sequencing of the gene encoding cytochrome C553 from Desulfovibrio vulgaris Hildenborough by Van Rooqen G. J. H. (1989)
  37. Voordouw , G. , and S. Brenner . 1986 . Cloning and sequencing of the gene encoding cytochrome C3 from Desulfovibrio vulgaris Hildenborough. Eur. J. Biochem. 159 : 347 - 351 . (10.1111/j.1432-1033.1986.tb09874.x) / Hildenborough. Eur. J. Biochem. / Cloning and sequencing of the gene encoding cytochrome C3 from Desulfovibrio vulgaris by Voordouw G. (1986)
  38. Voordouw , G. , V. Niviere , F. G. Ferris , P. M. Fedorak , and D. W. S. Westlake . 1990 . Distribution of hydrogenase genes in Desulfovibrio spp. and their use in identification of species from the oil field environment . Appl. Environ. Microbiol. 56 : 3748 - 3754 . (10.1128/AEM.56.12.3748-3754.1990) / Appl. Environ. Microbiol. / Distribution of hydrogenase genes in Desulfovibrio spp. and their use in identification of species from the oil field environment by Voordouw G. (1990)
  39. Voordouw , G. , W. B. R. Pollock , M. Bruschi , F. Guerlesquin , B. J. Rapp-Giles , and J. D. Wall . 1990 . Functional expression of Desulfovibrio vulgaris Hildenborough cytochrome C3 in Desulfovibrio desulfuricans G200 after conjugational gene transfer from Escherichia coli . J. Bacteriol. 172 : 6122 - 6126 . (10.1128/JB.172.10.6122-6126.1990) / J. Bacteriol. / Functional expression of Desulfovibrio vulgaris Hildenborough cytochrome C3 in Desulfovibrio desulfuricans G200 after conjugational gene transfer from Escherichia coli by Voordouw G. (1990)
  40. Voordouw , G. , J. D. Strang , and F. R. Wilson . 1989 . Organization of the genes encoding [Fe] hydrogenase in Desulfovibrio vulgaris subsp. oxamicus Monticello . J. Bacteriol. 171 : 3881 - 3889 . (10.1128/jb.171.7.3881-3889.1989) / J. Bacteriol. / Organization of the genes encoding [Fe] hydrogenase in Desulfovibrio vulgaris subsp. oxamicus Monticello by Voordouw G. (1989)
  41. Weber , P. C. , R. G. Bartsch , M. A. Cusanovich , R. C. Hamlin , A. Howard , S. R. Jordan , M. D. Kamen , T. E. Meyer , D. W. Weatherford , Nguyen huu Xuong, and F. R. Salemme . 1980 . Structure of cytochrome c': a dimeric high-spin haem protein . Nature (London) 286 : 302 - 304 . (10.1038/286302a0) / Nature (London) / Structure of cytochrome c': a dimeric high-spin haem protein by Weber P. C. (1980)
  42. Weimer , P. J. , M. J. Van Kavelaar , C. B. Michel , and T. K Ng. 1988 . Effect of phosphate on the corrosion of carbon steel and on the composition of corrosion products in two-stage continuous cultures of Desulfovibrio desulfuricans . Appl. Environ. Microbiol. 54 : 386 - 396 . (10.1128/aem.54.2.386-396.1988) / Appl. Environ. Microbiol. / Effect of phosphate on the corrosion of carbon steel and on the composition of corrosion products in two-stage continuous cultures of Desulfovibrio desulfuricans by Weimer P. J. (1988)
  43. Yamamoto , K. , R. M. Macnab , and Y. Imae . 1990 . Repellent response functions of the Trg and Tap chemoreceptors of Escherichia coli . J. Bacteriol. 172 : 383 - 388 . (10.1128/JB.172.1.383-388.1990) / J. Bacteriol. / Repellent response functions of the Trg and Tap chemoreceptors of Escherichia coli by Yamamoto K. (1990)
Dates
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Created 8 years, 9 months ago (Nov. 7, 2016, 2:07 p.m.)
Deposited 4 years ago (July 29, 2021, 1:19 p.m.)
Indexed 1 month, 4 weeks ago (June 25, 2025, 6:29 a.m.)
Issued 31 years, 7 months ago (Jan. 1, 1994)
Published 31 years, 7 months ago (Jan. 1, 1994)
Published Print 31 years, 7 months ago (Jan. 1, 1994)
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@article{Fu_1994, title={DcrA, a c-type heme-containing methyl-accepting protein from Desulfovibrio vulgaris Hildenborough, senses the oxygen concentration or redox potential of the environment}, volume={176}, ISSN={1098-5530}, url={http://dx.doi.org/10.1128/jb.176.2.344-350.1994}, DOI={10.1128/jb.176.2.344-350.1994}, number={2}, journal={Journal of Bacteriology}, publisher={American Society for Microbiology}, author={Fu, R and Wall, J D and Voordouw, G}, year={1994}, month=jan, pages={344–350} }