Genes Regulated by TorR, the Trimethylamine Oxide Response Regulator of Shewanella Oneidensis

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 2004 Jul 3

PMID 15231782

Citations 18

Authors

Christophe Bordi

Mireille Ansaldi

Stephanie Gon

Cecile Jourlin-Castelli

Chantal Iobbi-Nivol

Vincent Mejean

Affiliations

Soon will be listed here.

Abstract

The torECAD operon encoding the trimethylamine oxide (TMAO) respiratory system of Shewanella oneidensis is positively controlled by the TorS/TorR two-component system when TMAO is available. Activation of the tor operon occurs upon binding of the phosphorylated response regulator TorR to a single operator site containing the direct repeat nucleotide sequence TTCATAN4TTCATA. Here we show that the replacement of any nucleotide of one TTCATA hexamer prevented TorR binding in vitro, meaning that TorR specifically interacts with this DNA target. Identical direct repeat sequences were found in the promoter regions of torR and of the new gene torF (SO4694), and they allowed TorR binding to both promoters. Real-time PCR experiments revealed that torR is negatively autoregulated, whereas torF is strongly induced by TorR in response to TMAO. Transcription start site location and footprinting analysis indicate that the operator site at torR overlaps the promoter -10 box, whereas the operator site at torF is centered at -74 bp from the start site, in agreement with the opposite role of TorR in the regulation of the two genes. Since torF and torECAD are positively coregulated by TorR, we propose that the TorF protein plays a role related to TMAO respiration.

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References

Ansaldi M, Bordi C, Lepelletier M, Mejean V . TorC apocytochrome negatively autoregulates the trimethylamine N-oxide (TMAO) reductase operon in Escherichia coli. Mol Microbiol. 1999; 33(2):284-95. DOI: 10.1046/j.1365-2958.1999.01468.x. View

Hatton A, Gibb S . A technique for the determination of trimethylamine-N-oxide in natural waters and biological media. Anal Chem. 1999; 71(21):4886-91. DOI: 10.1021/ac990366y. View

Myers J, Myers C . Role of the tetraheme cytochrome CymA in anaerobic electron transport in cells of Shewanella putrefaciens MR-1 with normal levels of menaquinone. J Bacteriol. 1999; 182(1):67-75. PMC: 94241. DOI: 10.1128/JB.182.1.67-75.2000. View

Ansaldi M, Simon G, Lepelletier M, Mejean V . The TorR high-affinity binding site plays a key role in both torR autoregulation and torCAD operon expression in Escherichia coli. J Bacteriol. 2000; 182(4):961-6. PMC: 94371. DOI: 10.1128/JB.182.4.961-966.2000. View

Proctor L, Gunsalus R . Anaerobic respiratory growth of Vibrio harveyi, Vibrio fischeri and Photobacterium leiognathi with trimethylamine N-oxide, nitrate and fumarate: ecological implications. Environ Microbiol. 2001; 2(4):399-406. DOI: 10.1046/j.1462-2920.2000.00121.x. View

Hoffer S, Westerhoff H, Hellingwerf K, Postma P, Tommassen J . Autoamplification of a two-component regulatory system results in "learning" behavior. J Bacteriol. 2001; 183(16):4914-7. PMC: 99548. DOI: 10.1128/JB.183.16.4914-4917.2001. View

Gon S, Theraulaz L, Mejean V . An unsuspected autoregulatory pathway involving apocytochrome TorC and sensor TorS in Escherichia coli. Proc Natl Acad Sci U S A. 2001; 98(20):11615-20. PMC: 58778. DOI: 10.1073/pnas.211330598. View

Zou Q, Bennion B, Daggett V, Murphy K . The molecular mechanism of stabilization of proteins by TMAO and its ability to counteract the effects of urea. J Am Chem Soc. 2002; 124(7):1192-202. DOI: 10.1021/ja004206b. View

Gon S, Patte J, Mejean V . Reconstitution of the trimethylamine oxide reductase regulatory elements of Shewanella oneidensis in Escherichia coli. J Bacteriol. 2002; 184(5):1262-9. PMC: 134858. DOI: 10.1128/JB.184.5.1262-1269.2002. View

10.

Kenney L . Structure/function relationships in OmpR and other winged-helix transcription factors. Curr Opin Microbiol. 2002; 5(2):135-41. DOI: 10.1016/s1369-5274(02)00310-7. View

11.

Blanco A, Sola M, Gomis-Ruth F, Coll M . Tandem DNA recognition by PhoB, a two-component signal transduction transcriptional activator. Structure. 2002; 10(5):701-13. DOI: 10.1016/s0969-2126(02)00761-x. View

12.

Gram L, Dalgaard P . Fish spoilage bacteria--problems and solutions. Curr Opin Biotechnol. 2002; 13(3):262-6. DOI: 10.1016/s0958-1669(02)00309-9. View

13.

Heidelberg J, Paulsen I, Nelson K, Gaidos E, Nelson W, Read T . Genome sequence of the dissimilatory metal ion-reducing bacterium Shewanella oneidensis. Nat Biotechnol. 2002; 20(11):1118-23. DOI: 10.1038/nbt749. View

14.

Yancey P, Blake W, Conley J . Unusual organic osmolytes in deep-sea animals: adaptations to hydrostatic pressure and other perturbants. Comp Biochem Physiol A Mol Integr Physiol. 2002; 133(3):667-76. DOI: 10.1016/s1095-6433(02)00182-4. View

15.

Bordi C, Iobbi-Nivol C, Mejean V, Patte J . Effects of ISSo2 insertions in structural and regulatory genes of the trimethylamine oxide reductase of Shewanella oneidensis. J Bacteriol. 2003; 185(6):2042-5. PMC: 150150. DOI: 10.1128/JB.185.6.2042-2045.2003. View

16.

Bordi C, Theraulaz L, Mejean V, Jourlin-Castelli C . Anticipating an alkaline stress through the Tor phosphorelay system in Escherichia coli. Mol Microbiol. 2003; 48(1):211-23. DOI: 10.1046/j.1365-2958.2003.03428.x. View

17.

Minagawa S, Ogasawara H, Kato A, Yamamoto K, Eguchi Y, Oshima T . Identification and molecular characterization of the Mg2+ stimulon of Escherichia coli. J Bacteriol. 2003; 185(13):3696-702. PMC: 161583. DOI: 10.1128/JB.185.13.3696-3702.2003. View

18.

Robinson V, Wu T, Stock A . Structural analysis of the domain interface in DrrB, a response regulator of the OmpR/PhoB subfamily. J Bacteriol. 2003; 185(14):4186-94. PMC: 164896. DOI: 10.1128/JB.185.14.4186-4194.2003. View

19.

Bijlsma J, Groisman E . Making informed decisions: regulatory interactions between two-component systems. Trends Microbiol. 2003; 11(8):359-66. DOI: 10.1016/s0966-842x(03)00176-8. View

20.

Lejona S, Aguirre A, Cabeza M, Garcia Vescovi E, Soncini F . Molecular characterization of the Mg2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J Bacteriol. 2003; 185(21):6287-94. PMC: 219391. DOI: 10.1128/JB.185.21.6287-6294.2003. View