Coproporphyrin excretion and low thiol levels caused by point mutation in the Rhodobacter sphaeroides S-adenosylmethionine synthetase gene

Journal of Bacteriology

Volumn 192, Issue 5, 2010, Pages 1238-1248

  Sabaty, Monique ^a,b,c   Adryanczyk, Géraldine ^a,b,c   Roustan, Chloë ^a,b,c   Cuiné, Stephan ^a,b,c   Lamouroux, Christine ^d   Pignol, David ^a,b,c  

^a IRFM   (France)

^b CNRS   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d DIF   (France)

Author keywords

[No Author keywords available]

Indexed keywords

COPROPORPHYRIN; COPROPORPHYRINOGEN OXIDASE; CYSTEINE; CYSTEINE SYNTHASE; DIMETHYL SULFOXIDE; ENZYME; GLUTATHIONE; METHIONINE ADENOSYLTRANSFERASE; MOLYBDENUM COFACTOR BIOSYNTHESIS PROTEIN A; NITRATE REDUCTASE; S ADENOSYLMETHIONINE; THIOL; UNCLASSIFIED DRUG; UROPORPHYRINOGEN III METHYLTRANSFERASE;

AMINO ACID SUBSTITUTION; ARTICLE; ENZYME ACTIVITY; NONHUMAN; PLEIOTROPY; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; RHODOBACTER SPHAEROIDES; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; COPROPORPHYRINS; CYSTEINE; DNA MUTATIONAL ANALYSIS; DNA, BACTERIAL; GENETIC COMPLEMENTATION TEST; GLUTATHIONE; METHIONINE ADENOSYLTRANSFERASE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; POINT MUTATION; RHODOBACTER SPHAEROIDES; S-ADENOSYLMETHIONINE; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; SULFHYDRYL COMPOUNDS;

RHODOBACTER SPHAEROIDES; RHODOBACTER SPHAEROIDES F. SP. DENITRIFICANS;

EID: 77749298005     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01342-09     Document Type: Article

References (52)

1. Albanesi, D., M. C. Mansilla, G. E. Schujman, and D. de Mendoza. 2005. Bacillus subtilis cysteine synthetase is a global regulator of the expression of genes involved in sulfur assimilation. J. Bacteriol. 187:7631-7638.
2. Arnoux, P., M. Sabaty, J. Alric, B. Frangioni, B. Guigliarelli, J. M. Adriano, and D. Pignol. 2003. Structural and redox plasticity in the heterodimeric periplasmic nitrate reductase. Nat. Struct. Biol. 10:928-934.
3. Brokx, S. J., R. A. Rothery, G. Zhang, D. P. Ng, and J. H. Weiner. 2005. Characterization of an Escherichia coli sulfite oxidase homologue reveals the role of a conserved active site cysteine in assembly and function. Biochemistry 44:10339-10348.
4. Cantoni, G. L. 1975. Biological methylation: selected aspects. Annu. Rev. Biochem. 44:435-451.
5. Chartrand, P., D. Tardif, and A. Sasarman. 1979. Uroporphyrin- and coproporphyrin I-accumulating mutant of Escherichia coli K12. J. Gen. Microbiol. 110:61-66.
6. Chattopadhyay, A., M. Meier, S. Ivaninskii, P. Burkhard, F. Speroni, B. Campanini, S. Bettati, A. Mozzarelli, W. M. Rabeh, L. Li, and P. F. Cook. 2007. Structure, mechanism, and conformational dynamics of O-acetylserine sulfhydrylase from Salmonella typhimurium: comparison of A and B isozymes. Biochemistry 46:8315-8330.
7. Chiang, P. K., R. K. Gordon, J. Tal, G. C. Zeng, B. P. Doctor, K. Pardhasaradhi, and P. P. McCann. 1996. S-Adenosylmethionine and methylation. FASEB J. 10:471-480.
8. Chory, J., and S. Kaplan. 1983. Light-dependent regulation of the synthesis of soluble and intracytoplasmic membrane proteins of Rhodopseudomonas sphaeroides. J. Bacteriol. 153:465-474.
9. Coomber, S. A., R. M. Jones, P. M. Jordan, and C. N. Hunter. 1992. A putative anaerobic coproporphyrinogen III oxidase in Rhodobacter sphaeroides. I. Molecular cloning, transposon mutagenesis and sequence analysis of the gene. Mol. Microbiol. 6:3159-3169.
10. Danton, M., and C. K. Lim. 2004. Identification of monovinyl tripropionic acid porphyrins and metabolites from faeces of patients with hereditary coproporphyria by high-performance liquid chromatography/electrospray ionization quadrupole time-of-flight tandem mass spectrometry. Rapid Commun. Mass Spectrom. 18:2309-2316.
11. Dever, J. T., and A. A. Elfarra. 2006. In vivo metabolism of L-methionine in mice: evidence for stereoselective formation of methionine-D-sulfoxide and quantitation of other major metabolites. Drug Metab. Dispos. 34:2036-2043.
12. Driskell, L. O., A. M. Tucker, H. H. Winkler, and D. O. Wood. 2005. Rickettsial metK-encoded methionine adenosyltransferase expression in an Escherichia coli metK deletion strain. J. Bacteriol. 187:5719-5722.
13. Dryden, S. C., and S. Kaplan. 1990. Localization and structural analysis of the ribosomal RNA operons of Rhodobacter sphaeroides. Nucleic Acids Res. 18:7267-7277.
14. Fell, D. A. 1992. Metabolic control analysis: a survey of its theoretical and experimental development. Biochem. J. 286:313-330.
15. Fontecave, M., M. Atta, and E. Mulliez. 2004. S- adenosylmethionine: nothing goes to waste. Trends Biochem. Sci. 29:243-249.
16. Heinemann, I. U., M. Jahn, and D. Jahn. 2008. The biochemistry of heme biosynthesis. Arch. Biochem. Biophys. 474:238-251.
17. Hinchigeri, S. B., D. W. Nelson, and W. R. Richards. 1984. The purification and reaction mechanism of S-adenosyl-methionine:magnesium protoporphyrin methyltransferase from Rhodopseudomonas sphaeroides. Photosynthetica 18:168-178.
18. Inui, M., K. Nakata, J. H. Roh, A. A. Vertes, and H. Yukawa. 2003. Isolation and molecular characterization of pMG160, a mobilizable cryptic plasmid from Rhodobacter blasticus. Appl. Environ. Microbiol. 69:725-733.
19. Kiley, P. J., and S. Kaplan. 1988. Molecular genetics of photosynthetic membrane biosynthesis in Rhodobacter sphaeroides. Microbiol. Rev. 52:50-69.
20. Kovach, M. E., P. H. Elzer, D. S. Hill, G. T. Robertson, M. A. Farris, R. M. Roop II, and K. M. Peterson. 1995. Four new derivatives of the broad-hostrange cloning vector pBBR1MCS, carrying different antibiotic- resistance cassettes. Gene 166:175-176.
21. Kredich, N. M. 1996. Biosynthesis of cysteine, p. 514-527. In F. C. Neidhardt, R. Curtiss III, J. L. Ingraham, E. C. C. Lin, K. B. Low, B. Magasanik, W. S. Reznikoff, M. Riley, M. Schaechter, and H. E. Umbarger (ed.), Escherichia coli and Salmonella: cellular and molecular biology, 2nd ed., vol. 1. American Society for Microbiology, Washington, DC.
22. Kristjansson, J. K., and T. C. Hollocher. 1980. First practical assay for soluble nitrous oxide reductase of denitrifying bacteria and a partial kinetic characterization. J. Biol. Chem. 255:704-707.
23. Lascelles, J. 1959. Adaptation to form bacteriochlorophyll in Rhodopseudomonas spheroides: changes in activity of enzymes concerned in pyrrole synthesis. Biochem. J. 72:508-518.
24. Layer, G., J. Moser, D. W. Heinz, D. Jahn, and W. D. Schubert. 2003. Crystal structure of coproporphyrinogen III oxidase reveals cofactor geometry of radical SAM enzymes. EMBO J. 22:6214-6224.
25. Lieb, C., R. A. Siddiqui, B. Hippler, D. Jahn, and B. Friedrich. 1998. The Alcaligenes eutrophus hemN gene encoding the oxygen-independent coproporphyrinogen III oxidase, is required for heme biosynthesis during anaerobic growth. Arch. Microbiol. 169:52-60.
26. Lithgow, J. K., E. J. Hayhurst, G. Cohen, Y. Aharonowitz, and S. J. Foster. 2004. Role of a cysteine synthase in Staphylococcus aureus. J. Bacteriol. 186:1579-1590.
27. Miyamoto, K., K. Nishimura, T. Masuda, H. Tsuji, and H. Inokuchi. 1992. Accumulation of protoporphyrin IX in light-sensitive mutants of Escherichia coli. FEBS Lett. 310:246-248.
28. Newman, E. B., L. I. Budman, E. C. Chan, R. C. Greene, R. T. Lin, C. L. Woldringh, and R. D'Ari. 1998. Lack of S-adenosylmethionine results in a cell division defect in Escherichia coli. J. Bacteriol. 180:3614-3619.
29. O'Gara, J. P., M. Gomelsky, and S. Kaplan. 1997. Identification and molecular genetic analysis of multiple loci contributing to high-level tellurite resistance in Rhodobacter sphaeroides 2.4.1. Appl. Environ. Microbiol. 63: 4713-4720.
30. Oh, J. I., J. M. Eraso, and S. Kaplan. 2000. Interacting regulatory circuits involved in orderly control of photosynthesis gene expression in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 182:3081-3087.
31. Prentki, P., and H. M. Krisch. 1984. In vitro insertional mutagenesis with a selectable DNA fragment. Gene 29:303-313.
32. Quandt, J., and M. F. Hynes. 1993. Versatile suicide vectors which allow direct selection for gene replacement in gram-negative bacteria. Gene 127: 15-21.
33. Rijstenbil, J. W., and J. A. Wijnholds. 1996. HPLC analysis of nonprotein thiols in planktonic diatoms: pool size, redox state and response to copper and cadmium exposure. Mar. Biol. 127:45-54.
34. Sander, J., and C. Dahl. 2009. Metabolism of inorganic sulfur compounds in purple bacteria, p. 595-622. In C. N. Hunter, F. Daldal, M. C. Thurnauer, and J. T. Beatty, (ed.), The purple phototrophic bacteria. Springer Netherlands, Dordrecht, The Netherlands.
35. Sasarman, A., P. Chartrand, R. Proschek, M. Desrochers, D. Tardif, and C. Lapointe. 1975. Uroporphyrin-accumulating mutant of Escherichia coli K-12. J. Bacteriol. 124:1205-1212.
36. Sasarman, A., and M. Desrochers. 1976. Uroporphyrinogen III cosynthasedeficient mutant of Salmonella typhimurium LT2. J. Bacteriol. 128:717-721.
37. Sasarman, A., M. Desrochers, S. Sonea, K. E. Sanderson, and M. Surdeanu. 1976. Porphobilinogen-accumulating mutants of Salmonella typhimurium LT2. J. Gen. Microbiol. 94:359-366.
38. Shi, W., and D. R. Zusman. 1995. Methionine inhibits developmental aggregation of Myxococcus xanthus by blocking the biosynthesis of S-adenosyl methionine. J. Bacteriol. 177:5346-5349.
39. Sistrom, W. R. 1977. Transfer of chromosomal genes mediated by plasmid r68.45 in Rhodopseudomonas sphaeroides. J. Bacteriol. 131:526-532.
40. Sofia, H. J., G. Chen, B. G. Hetzler, J. F. Reyes-Spindola, and N. E. Miller. 2001. Radical SAM, a novel protein superfamily linking unresolved steps in familiar biosynthetic pathways with radical mechanisms: functional characterization using new analysis and information visualization methods. Nucleic Acids Res. 29:1097-1106.
41. Takusagawa, F., S. Kamitori, and G. D. Markham. 1996. Structure and function of S-adenosylmethionine synthetase: crystal structures of S-adenosylmethionine synthetase with ADP, BrADP, and PPi at 28 angstroms resolution. Biochemistry 35:2586-2596.
42. Tucker, A. M., H. H. Winkler, L. O. Driskell, and D. O. Wood. 2003. S-Adenosylmethionine transport in Rickettsia prowazekii. J. Bacteriol. 185: 3031-3035.
43. Vergnes, A., K. Gouffi-Belhabich, F. Blasco, G. Giordano, and A. Magalon. 2004. Involvement of the molybdenum cofactor biosynthetic machinery in the maturation of the Escherichia coli nitrate reductase A. J. Biol. Chem. 279:41398-41403.
44. Warren, M. J., and E. Deery. 2009. Vitamin B12 (cobalamin) biosynthesis in the purple bacteria, p. 81-95. In C. N. Hunter, F. Daldal, M. C. Thurnauer, and J. T. Beatty, (ed.), The purple phototrophic bacteria. Springer Netherlands, Dordrecht, The Netherlands.
45. Wei, Y., and E. B. Newman. 2002. Studies on the role of the metK gene product of Escherichia coli K-12. Mol. Microbiol. 43:1651-1656.
46. Willows, R. D., and A. M. Kriegel. 2009. Biosynthesis of bacteriochlorophyll in purple bacteria, p. 57-79. In C. N. Hunter, F. Daldal, M. C. Thurnauer, and J. T. Beatty, (ed.), The purple phototrophic bacteria. Springer Netherlands, Dordrecht, The Netherlands.
47. Wright, D. J., J. M. Rideout, and C. K. Lim. 1983. High-performance liquid chromatography of coproporphyrin isomers. Biochem. J. 209:553-555.
48. Xu, K., J. Delling, and T. Elliott. 1992. The genes required for heme synthesis in Salmonella typhimurium include those encoding alternative functions for aerobic and anaerobic coproporphyrinogen oxidation. J. Bacteriol. 174:3953-3963.
49. Yocum, R. R., J. B. Perkins, C. L. Howitt, and J. Pero. 1996. Cloning and characterization of the metE gene encoding S-adenosylmethionine synthetase from Bacillus subtilis. J. Bacteriol. 178:4604-4610.
50. Zeilstra-Ryalls, J. 2009. Regulation of the tetrapyrolle biosynthetic pathway, p. 777-798. In C. N. Hunter, F. Daldal, M. C. Thurnauer, and J. T. Beatty, (ed.), The purple phototrophic bacteria. Springer Netherlands, Dordrecht, The Netherlands.
51. Zeilstra-Ryalls, J. H., and S. Kaplan. 1995. Aerobic and anaerobic regulation in Rhodobacter sphaeroides 2.4.1: the role of the fnrL gene. J. Bacteriol. 177:6422-6431.
52. Zeng, X., and S. Kaplan. 2001. TspO as a modulator of the repressor/antirepressor (PpsR/AppA) regulatory system in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 183:6355-6364.