The anaerobe-specific orange protein complex of Desulfovibrio vulgaris hildenborough is encoded by two divergent operons coregulated by σ54 and a cognate transcriptional regulator

Journal of Bacteriology

Volumn 193, Issue 13, 2011, Pages 3207-3219

  Fiévet, Anouchka ^a   My, Laetitia ^a   Cascales, Eric ^b   Ansaldi, Mireille ^c   Pauleta, Sofia R ^d   Moura, Isabel ^d   Dermoun, Zorah ^a   Bernard, Christophe S ^b   Dolla, Alain ^a   Aubert, Corinne ^a  

^a CNRS and Aix Marseille University   (France)

^b CNRS   (France)

^c AIX MARSEILLE UNIVERSITÉ   (France)

^d UNIVERSIDADE NOVA DE LISBOA   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

RNA POLYMERASE;

ANAEROBE; ARTICLE; BACTERIAL CELL; BACTERIAL GENOME; BACTERIAL STRAIN; CONTROLLED STUDY; DESULFOVIBRIO VULGARIS; GENE CLUSTER; GENE INSERTION; METHANOSARCINA BARKERI; NONHUMAN; OPERON; PRIORITY JOURNAL; PROMOTER REGION; SEQUENCE ANALYSIS; STRUCTURAL GENE; TRANSCRIPTION REGULATION;

BACTERIA (MICROORGANISMS); DESULFOVIBRIO VULGARIS SUBSP. VULGARIS STR. HILDENBOROUGH;

EID: 79959338188     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.00044-11     Document Type: Article

References (59)

1. Ansaldi, M., G. Simon, M. Lepelletier, and V. Méjean. 2000. The TorR high-affinity binding site plays a key role in both torR autoregulation and torCAD operon expression in Escherichia coli. J. Bacteriol. 182:961-966.
2. Aschtgen, M. S., M. Gavioli, A. Dessen, R. Lloubès, and E. Cascales. 2010. The SciZ protein anchors the enteroaggregative Escherichia coli type VI secretion system to the cell wall. Mol. Microbiol. 75:886-899.
3. Barton, L., and G. Fauque. 2009. Biochemistry, physiology and biotechnology of sulfate-reducing bacteria. Adv. Appl. Microbiol. 68:41-98.
4. Bernard, C. S., Y. R. Brunet, M. Gavioli, R. Lloubès, and E. Cascales. 2011. Regulation of type VI secretion gene clusters by sigma54 and cognate enhancer binding proteins. J. Bacteriol. 193:2158-2167.
5. Bose, D., et al. 2008. Organization of an activator-bound RNA polymerase holoenzyme. Mol. Cell 32:337-346.
6. Brockhurst, M. A., N. Colegrave, and D. E. Rozen. 2011. Next-generation sequencing as a tool to study microbial evolution. Mol. Ecol. 20:972-980.
7. Buck, M., M. T. Gallegos, D. J. Studholme, Y. Guo, and J. D. Gralla. 2000. The bacterial enhancer-dependent sigma(54) (sigma(N)) transcription factor. J. Bacteriol. 182:4129-4136.
8. Bursakov, S. A., et al. 2004. Antagonists Mo and Cu in a heterometallic cluster present on a novel protein (orange protein) isolated from Desulfovibrio gigas. J. Inorg. Biochem. 98:833-840.
9. Calogero, S., et al. 1994. RocR, a novel regulatory protein controlling arginine utilization in Bacillus subtilis, belongs to the NtrC/NifA family of transcriptional activators. J. Bacteriol. 176:1234-1241.
10. Chhabra, S., et al. 2006. Global analysis of heat shock response in Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 188:1817-1828.
11. Christie, J. M., et al. 1998. Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. Science 282:1698-1701.
12. Columbus, L., W. Peti, T. Etezady-Esfarjani, T. Herrmann, and K. Wüthrich. 2005. NMR structure determination of the conserved hypothetical protein TM1816 from Thermotoga maritima. Proteins 60:552-557.
13. Cort, J., A. Yee, A. Edwards, C. Arrowsmith, and M. Kennedy. 2000. NMR structure determination and structure-based functional characterization of conserved hypothetical protein MTH1175 from Methanobacterium thermoautotrophicum. J. Struct. Funct. Genomics 1:15-25.
14. Datsenko, K. A., and B. L. Wanner. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc. Natl. Acad. Sci. U. S. A. 97:6640-6645.
15. David, M.,et al. 1988. Cascade regulation of nif gene expression in Rhizobium meliloti. Cell 54:671-683.
16. Debarbouille, M., R. Gardan, M. Arnaud, and G. Rapoport. 1999. Role of bkdR, a transcriptional activator of the sigL-dependent isoleucine and valine degradation pathway in Bacillus subtilis. J. Bacteriol. 181:2059-2066.
17. de Boer, P. A., R. E. Crossley, and L. I. Rothfield. 1989. A division inhibitor and a topological specificity factor coded for by the minicell locus determine proper placement of the division septum in E. coli. Cell 56:641-649.
18. Dermoun, Z., et al. 2010. TM0486 from the hyperthermophilic anaerobe Thermotoga maritima is a thiamin-binding protein involved in response of the cell to oxidative conditions. J. Mol. Biol. 400:463-476.
19. Elias, D., et al. 2009. Expression profiling of hypothetical genes in Desulfovibrio vulgaris leads to improved functional annotation. Nucleic Acids Res. 37:2926-2939.
20. Etezady-Esfarjani, T., et al. 2004. NMR structure determination of the hypothetical protein TM1290 from Thermotoga maritima using automated NOESY analysis. J. Biomol. NMR 29:403-406.
21. Finn, R. D., et al. 2006. Pfam: clans, web tools and services. Nucleic Acids Res. 34:D247-D251.
22. García-Moreno, D., et al. 2009. A vitamin B12-based system for conditional expression reveals dksA to be an essential gene in Myxococcus xanthus. J. Bacteriol. 191:3108-3119.
23. Gardan, R., G. Rapoport, and M. Débarbouillé. 1997. Role of the transcriptional activator RocR in the arginine-degradation pathway of Bacillus subtilis. Mol. Microbiol. 24:825-837.
24. George, G. N., et al. 2000. A novel protein-bound copper-molybdenum cluster. J. Am. Chem. Soc. 122:8321-8832.
25. Guiral, M., et al. 2009. New insights into the respiratory chains of the chemolithoautotrophic and hyperthermophilic bacterium Aquifex aeolicus. J. Proteome Res. 8:1717-1730.
26. Hansen, T. 1994. Metabolism of sulfate-reducing prokaryotes. Antonie Van Leeuwenhoek 66:165-185.
27. Heidelberg, J., et al. 2004. The genome sequence of the anaerobic, sulfatereducing bacterium Desulfovibrio vulgaris Hildenborough. Nat. Biotechnol. 22:554-559.
28. Hillesland, K. L., and D. A. Stahl. 2010. Rapid evolution of stability and productivity at the origin of a microbial mutualism. Proc. Natl. Acad. Sci. U. S. A. 107:2124-2129.
29. Jefferson, R. A., S. M. Burgess, and D. Hirsh. 1986. Beta-glucuronidase from Escherichia coli as a gene-fusion marker. Proc. Natl. Acad. Sci. U. S. A. 83:8447-8451.
30. Jelsbak, L., M. Givskov, and D. Kaiser. 2005. Enhancer-binding proteins with a forkhead-associated domain and the sigma54 regulon in Myxococcus xanthus fruiting body development. Proc. Natl. Acad. Sci. U. S. A. 102:3010-3015.
31. Kroos, L. 2005. Eukaryotic-like signaling and gene regulation in a prokaryote that undergoes multicellular development. Proc. Natl. Acad. Sci. U. S. A. 102:2681-2682.
32. Lutkenhaus, J. 2007. Assembly dynamics of the bacterial MinCDE system and spatial regulation of the Z ring. Annu. Rev. Biochem. 76:539-562.
33. Martínez, M., M. V. Colombo, J. M. Palacios, J. Imperial, and T. Ruiz-Argüeso. 2008. Novel arrangement of enhancer sequences for NifA-dependent activation of the hydrogenase gene promoter in Rhizobium leguminosarum bv. viciae. J. Bacteriol. 190:3185-3191.
34. Meier, T., P. Schickor, A. Wedel, L. Cellai, and H. Heumann. 1995. In vitro transcription close to the melting point of DNA: analysis of Thermotoga maritima RNA polymerase-promoter complexes at 75 degrees C using chemical probes. Nucleic Acids Res. 23:988-994.
35. Merrick, M. J. 1993. In a class of its own-the RNA polymerase sigma factor sigma 54 (sigma N). Mol. Microbiol. 10:903-909.
36. Miller, J. H. 1975. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
37. Möglich, A., R. A. Ayers, and K. Moffat. 2009. Structure and signaling mechanism of Per-ARNT-Sim domains. Structure 17:1282-1294.
38. Morais Cabral, J. H., et al. 1998. Crystal structure and functional analysis of the HERG potassium channel N terminus: a eukaryotic PAS domain. Cell 95:649-655.
39. Morett, E., and L. Segovia. 1993. The sigma 54 bacterial enhancer-binding protein family: mechanism of action and phylogenetic relationship of their functional domains. J. Bacteriol. 175:6067-6074.
40. Muyzer, G., and A. J. Stams. 2008. The ecology and biotechnology of sulphate-reducing bacteria. Nat. Rev. Microbiol. 6:441-454.
41. Nambu, J. R., J. O. Lewis, K. A. Wharton, and S. T. Crews. 1991. The Drosophila single-minded gene encodes a helix-loop-helix protein that acts as a master regulator of CNS midline development. Cell 67:1157-1167.
42. Pauleta, S., et al. 2007. NMR assignment of the apo-form of a Desulfovibrio gigas protein containing a novel Mo-Cu cluster. Biomol. NMR Assign. 1:81-83.
43. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
44. Popham, D. L., D. Szeto, J. Keener, and S. Kutsu. 1989. Function of a bacterial activator protein that binds to transcriptional enhancers. Science 243:629-635.
45. Postgate, J. 1966. Media for sulphur bacteria. Lab. Pract. 15:1239-1244.
46. Rothfield, L., A. Taghbalout, and Y. L. Shih. 2005. Spatial control of bacterial division-site placement. Nat. Rev. Microbiol. 3:959-968.
47. Sasse-Dwight, S., and J. D. Gralla. 1990. Role of eukaryotic-type functional domains found in the prokaryotic enhancer receptor factor sigma 54. Cell 62:945-954.
48. Schleif, R. 2000. Regulation of the L-arabinose operon of Escherichia coli. Trends Genet. 16:559-565.
49. Schmidt, T. G., and A. Skerra. 2007. The Strep-tag system for one-step purification and high-affinity detection or capturing of proteins. Nat. Protoc. 2:1528-1535.
50. Scholten, J., D. Culley, F. Brockman, G. Wu, and W. Zhang. 2007. Evolution of the syntrophic interaction between Desulfovibrio vulgaris and Methanosarcina barkeri: involvement of an ancient horizontal gene transfer. Biochem. Biophys. Res. Commun. 352:48-54.
51. Studholme, D. J., and R. Dixon. 2003. Domain architectures of sigma54-dependent transcriptional activators. J. Bacteriol. 185:1757-1767.
52. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. U. S. A. 82:1074-1078.
53. Tatusov, R. L., E. V. Koonin, and D. J. Lipman. 1997. A genomic perspective on protein families. Science 278:631-637.
54. Taylor, B. L., and I. B. Zhulin. 1999. PAS domains: internal sensors of oxygen, redox potential, and light. Microbiol. Mol. Biol. Rev. 63:479-506.
55. van den Ent, F., and J. Löwe. 2006. RF cloning: a restriction-free method for inserting target genes into plasmids. J. Biochem. Biophys. Methods 67:67-74.
56. Vieira, J., and J. Messing. 1991. New pUC-derived cloning vectors with different selectable markers and DNA replication origins. Gene 100:189-194.
57. Voordouw, G., et al. 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.
58. Walker, C., et al. 2009. The electron transfer system of syntrophically grown Desulfovibrio vulgaris. J. Bacteriol. 191:5793-5801.
59. Wedel, A., and S. Kutsu. 1995. The bacterial enhancer-binding protein NTRC is a molecular machine: ATP hydrolysis is coupled to transcriptional activation. Genes Dev. 9:2042-2052.