journal article Aug 15, 2006

The Nitric Oxide-Responsive Regulator NsrR Controls ResDE-Dependent Gene Expression

View at Publisher Save 10.1128/jb.00486-06
Abstract
ABSTRACTThe ResD-ResE signal transduction system is essential for aerobic and anaerobic respiration inBacillus subtilis. ResDE-dependent gene expression is induced by oxygen limitation, but full induction under anaerobic conditions requires nitrite or nitric oxide (NO). Here we report that NsrR (formerly YhdE) is responsible for the NO-dependent up-regulation of the ResDE regulon. The null mutation ofnsrRled to aerobic derepression ofhmp(flavohemoglobin gene) partly in a ResDE-independent manner. In addition to its negative role in aerobichmpexpression, NsrR plays an important role under anaerobic conditions for regulation of ResDE-controlled genes, includinghmp. ResDE-dependent gene expression was increased by thensrRmutation in the absence of NO, but the expression was decreased by the mutation when NO was present. Consequently,B. subtiliscells lacking NsrR no longer sense and respond to NO (and nitrite) to up-regulate the ResDE regulon. Exposure to NO did not significantly change the cellular concentration of NsrR, suggesting that NO likely modulates the activity of NsrR. NsrR is similar to the recently described nitrite- or NO-sensitive transcription repressors present in various bacteria. NsrR likely has an Fe-S cluster, and interaction of NO with the Fe-S center is proposed to modulate NsrR activity.
Topics

No keywords indexed for this article. Browse by subject →

References
41
[1]
Akaike, T., M. Yoshida, Y. Miyamoto, K. Sato, M. Kohno, K. Sasamoto, K. Miyazaki, S. Ueda, and H. Maeda. 1993. Antagonistic action of imidazolineoxyl N-oxides against endothelium-derived relaxing factor/.NO through a radical reaction. Biochemistry 32 : 827-832. 10.1021/bi00054a013
[3]
Arai, H., M. Mizutani, and Y. Igarashi. 2003. Transcriptional regulation of the nos genes for nitrous oxide reductase in Pseudomonas aeruginosa. Microbiology 149 : 29-36. 10.1099/mic.0.25936-0
[5]
Beaumont, H. J., S. I. Lens, W. N. Reijnders, H. V. Westerhoff, and R. J. van Spanning. 2004. Expression of nitrite reductase in Nitrosomonas europaea involves NsrR, a novel nitrite-sensitive transcription repressor. Mol. Microbiol. 54 : 148-158. 10.1111/j.1365-2958.2004.04248.x
[7]
Bogdan, C. 2001. Nitric oxide and the regulation of gene expression. Trends Cell Biol. 11 : 66-75. 10.1016/s0962-8924(00)01900-0
[8]
Corker, H., and R. K. Poole. 2003. Nitric oxide formation by Escherichia coli. Dependence on nitrite reductase, the NO-sensing regulator Fnr, and flavohemoglobin Hmp. J. Biol. Chem. 278 : 31584-31592. 10.1074/jbc.m303282200
[9]
Cruz-Ramos, H., J. Crack, G. Wu, M. N. Hughes, C. Scott, A. J. Thomson, J. Green, and R. K. Poole. 2002. NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. EMBO J. 21 : 3235-3244. 10.1093/emboj/cdf339
[10]
D'Autreaux, B., D. Touati, B. Bersch, J. M. Latour, and I. Michaud-Soret. 2002. Direct inhibition by nitric oxide of the transcriptional ferric uptake regulation protein via nitrosylation of the iron. Proc. Natl. Acad. Sci. USA 99 : 16619-16624. 10.1073/pnas.252591299
[11]
D'Autreaux, B., N. P. Tucker, R. Dixon, and S. Spiro. 2005. A non-haem iron centre in the transcription factor NorR senses nitric oxide. Nature 437 : 769-772. 10.1038/nature03953
[12]
Ding, H., and B. Demple. 2000. Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. USA 97 : 5146-5150. 10.1073/pnas.97.10.5146
[15]
Giel, J. L., D. Rodionov, M. Liu, F. R. Blattner, and P. J. Kiley. 2006. IscR-dependent gene expression links iron-sulphur cluster assembly to the control of O2-regulated genes in Escherichia coli. Mol. Microbiol. 60 : 1058-1075. 10.1111/j.1365-2958.2006.05160.x
[16]
Goldstein, S., A. Russo, and A. Samuni. 2003. Reactions of PTIO and carboxy-PTIO with *NO, *NO2, and O2−*. J. Biol. Chem. 278 : 50949-50955. 10.1074/jbc.m308317200
[17]
Hayashi, K., T. Kensuke, K. Kobayashi, N. Ogasawara, and M. Ogura. 2006. Bacillus subtilis RghR (YvaN) represses rapG and rapH, which encode inhibitors of expression of the srfA operon. Mol. Microbiol. 59 : 1714-1729. 10.1111/j.1365-2958.2006.05059.x
[20]
Keon, R. G., R. Fu, and G. Voordouw. 1997. Deletion of two downstream genes alters expression of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough. Arch. Microbiol. 167 : 376-383. 10.1007/s002030050458
[21]
Kwiatkowski, A. V., and J. P. Shapleigh. 1996. Requirement of nitric oxide for induction of genes whose products are involved in nitric oxide metabolism in Rhodobacter sphaeroides 2.4.3. J. Biol. Chem. 271 : 24382-24388. 10.1074/jbc.271.40.24382
[23]
Miller J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory Press Cold Spring Harbor N.Y.
[29]
Nakano, M. M., Y. Zhu, M. LaCelle, X. Zhang, and F. M. Hulett. 2000. Interaction of ResD with regulatory regions of anaerobically induced genes in Bacillus subtilis. Mol. Microbiol. 37 : 1198-1207. 10.1046/j.1365-2958.2000.02075.x
[31]
Nakano, S., K. N. Erwin, M. Ralle, and P. Zuber. 2005. Redox-sensitive transcriptional control by thiol/disulphide switch in the global regulator, Spx. Mol. Microbiol. 55 : 498-510. 10.1111/j.1365-2958.2004.04395.x
[32]
Pohlmann, A., R. Cramm, K. Schmelz, and B. Friedrich. 2000. A novel NO-responding regulator controls the reduction of nitric oxide in Ralstonia eutropha. Mol. Microbiol. 38 : 626-638. 10.1046/j.1365-2958.2000.02157.x
[33]
Qi, Y., and F. M. Hulett. 1998. PhoP-P and RNA polymerase σA holoenzyme are sufficient for transcription of Pho regulon promoters in Bacillus subtilis: Pho-P activator sites within the coding region stimulate transcription in vitro. Mol. Microbiol. 28 : 1187-1197. 10.1046/j.1365-2958.1998.00882.x
[34]
Rodionov, D. A., I. L. Dubchak, A. P. Arkin, E. J. Alm, and M. S. Gelfand. 2005. Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLOS Comput. Biol. 1 : e55. 10.1371/journal.pcbi.0010055
[35]
Schwartz, C. J., J. L. Giel, T. Patschkowski, C. Luther, F. J. Ruzicka, H. Beinert, and P. J. Kiley. 2001. IscR, an Fe-S cluster-containing transcription factor, represses expression of Escherichia coli genes encoding Fe-S cluster assembly proteins. Proc. Natl. Acad. Sci. USA 98 : 14895-14900. 10.1073/pnas.251550898
[36]
Stamler, J. S., S. Lamas, and F. C. Fang. 2001. Nitrosylation. the prototypic redox-based signaling mechanism. Cell 106 : 675-683. 10.1016/s0092-8674(01)00495-0
[37]
Sun, G., S. M. Birkey, and F. M. Hulett. 1996. Three two-component signal-transduction systems interact for Pho regulation in Bacillus subtilis. Mol. Microbiol. 19 : 942-948.
[38]
Todd, J. D., M. Wexler, G. Sawers, K. H. Yeoman, P. S. Poole, and A. W. Johnston. 2002. RirA, an iron-responsive regulator in the symbiotic bacterium Rhizobium leguminosarum. Microbiology 148 : 4059-4071. 10.1099/00221287-148-12-4059
[41]
Yeoman, K. H., A. R. Curson, J. D. Todd, G. Sawers, and A. W. Johnston. 2004. Evidence that the Rhizobium regulatory protein RirA binds to cis-acting iron-responsive operators (IROs) at promoters of some Fe-regulated genes. Microbiology 150 : 4065-4074. 10.1099/mic.0.27419-0