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NsrR DNA-binding transcriptional repressor

Synonyms: NsrR, NsrR-nitric oxide, NsrR-[2Fe-2S]reduced, NsrR-[2Fe-2S]2+ oxidized
Summary:
NsrR, the "nitrite-sensitive repressor" [], regulates genes involved in cell protection against nitric oxide (NO) [1, 7]. A microarray analysis showed that this protein regulates directly or indirectly at least 30 genes, some of which are involved in protection against reactive nitrogen species that can be generated by NO [8]. A ChIP-chip analysis (chromatin immunoprecipitation and microarray analysis) revealed that NsrR regulates, in addition, genes involved in motility and/or biofilm development [5]. NsrR also appears to regulate σE-dependent genes in an RseA-independent manner [10]. NsrR belongs to the Rrf2 family [], which includes among others the [2Fe-2S]-containing transcription factor IscR and the iron regulator RirA [12].
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Transcription factor      
TF conformation(s):
Name Conformation Type TF-Effector Interaction Type Apo/Holo Conformation Evidence (Confirmed, Strong, Weak) References
NsrR Functional   [APPHINH], [HIFS], [IEP], [IPI] [1], [2], [3], [4], [5]
NsrR-[2Fe-2S]2+ oxidized Non-Functional Covalent Apo [BPP] [6]
NsrR-[2Fe-2S]reduced Functional Covalent Holo [BPP] [6]
NsrR-nitric oxide Non-Functional   nd nd
Evolutionary Family: Rrf2
Connectivity class: Local Regulator
Gene name: nsrR
  Genome position: 4406190-4406615
  Length: 426 bp / 141 aa
Operon name: nsrR-rnr-rlmB-yjfIJ
TU(s) encoding the TF:
Transcription unit        Promoter
nsrR-rnr-rlmB-yjfI
nsrRp


Regulon       
Regulated gene(s) aceE, aceF, bamE, bdcA, cdd, dkgB, dsdC, feaB, feaR, fhlA, fliA, fliZ, grxD, hcp, hcr, hmp, hycA, hycB, hycC, hycD, hycE, hycF, hycG, hycH, hycI, hypA, hypB, hypC, hypD, hypE, ihfA, infC, lrp, mepH, mhpT, ndh, norR, nrfA, nrfB, nrfC, nrfD, nrfE, nrfF, nrfG, pgpC, pheM, pheS, pheT, poxB, rfe, rffC, rffG, rffH, rffM, rffT, rplT, rpmI, rybB, sodB, sufA, sufB, sufC, sufD, sufE, sufS,
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Multifun term(s) of regulated gene(s) MultiFun Term (List of genes associated to the multifun term)
membrane (16)
anaerobic respiration (11)
enterobacterial common antigen (surface glycolipid) (11)
surface antigens (ECA, O antigen of LPS) (11)
fermentation (10)
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Regulated operon(s) bamE, bdcA, cdd, dkgB, dsdC, feaB, feaR, fliAZ-tcyJ, grxD, hcp-hcr-poxB-ltaE-ybjT, hmp, hycABCDEFGHI, hypABCDE-fhlA, lrp, mepH, mhpT, ndh, norR, nrfABCDEFG, pdhR-aceEF-lpd, pgpC-tadA, rfe-wzzE-wecBC-rffGHC-wecE-wzxE-rffT-wzyE-rffM, rybB, sodB, sufABCDSE, tehAB, thrS-infC-rpmI-rplT-pheMST-ihfA, tsgA, waaH, ydbD, yeaE, yeaR-yoaG, ygbA, ytfE
First gene in the operon(s) aceE, bamE, bdcA, cdd, dkgB, dsdC, feaB, feaR, fliA, fliA, grxD, hcp, hcp, hmp, hycA, hypA, hypA, lrp, mepH, mhpT, ndh, norR, nrfA, pgpC, rfe, rybB, sodB, sufA, tehA, thrS, thrS, tsgA, waaH, ydbD, yeaE, yeaR, ygbA, ytfE
Simple and complex regulons ArcA,FNR,Fis,Fur,IHF,NsrR,PdhR
ArcA,FNR,NsrR
CRP,CytR,NsrR
CRP,FeaR,NsrR
CRP,IHF,NsrR
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Simple and complex regulatory phrases Regulatory phrase (List of promoters regulated by the phrase)
[NsrR,-](34)


Transcription factor regulation    


Transcription factor binding sites (TFBSs) arrangements
      

  Functional conformation Function Promoter Sigma factor Central Rel-Pos Distance to first Gene Genes Sequence LeftPos RightPos Evidence (Confirmed, Strong, Weak) References
  NsrR repressor aceEp Sigma70, Sigma38 -81.0 -128.5 aceE, aceF
aattatccagAAGATGTTGTAaatcaagcgc
122883 122894 [GEA], [HIBSCS] [5]
  NsrR repressor bamEp Sigma24 67.0 -52.5 bamE
gtctattatcATCGGCATATTacagatgagc
2753547 2753558 [GEA], [HIBSCS] [5]
  NsrR repressor bdcAp Sigma70 -18.0 -29.5 bdcA
tttattatgtAACATGCATTAcaaaactgtt
4474077 4474088 [GEA], [HIBSCS] [5]
  NsrR repressor cddp Sigma70 9.0 -16.5 cdd
gttatcccatTACATGATTATgaggcaacgc
2231822 2231833 [GEA], [HIBSCS] [5]
  NsrR repressor dkgBp Sigma38 -11.0 -79.5 dkgB
cgcaaaaatcCTCTGCATTTTacgctctttt
229082 229093 [GEA], [HIBSCS] [5]
  NsrR repressor dkgBp Sigma38 64.0 -5.5 dkgB
tagcattaaaAGAGGCATATTatggctatcc
229156 229167 [GEA], [HIBSCS] [5]
  NsrR repressor dsdCp Sigma70 14.0 -104.5 dsdC
cttcatttttAGATGTAAATCactccattga
2477728 2477739 [GEA], [HIBSCS] [5]
  NsrR repressor feaBp1 Sigma70 -184.0 -210.5 feaB
tcgctctgtgAAATGTATTTTtattgttgca
1447303 1447314 [GEA], [HIBSCS] [5], [7]
  NsrR repressor feaRp2 Sigma70 2.0 -25.5 feaR
tcgctctgtgAAATGTATTTTtattgttgca
1447303 1447314 [GEA], [HIBSCS] [5]
  NsrR repressor fliAp1 Sigma70 -207.0 -237.5 fliA, fliZ, tcyJ
caaattcaatAAATTGCAATTcaacttgtag
2002021 2002032 [GEA], [HIBSCS] [5]
  NsrR repressor fliAp1 Sigma70 7.0 -24.5 fliA, fliZ, tcyJ
gccctgcgttATATGAGTTATcggcatgatt
2001808 2001819 [GEA], [HIBSCS], [SM] [5]
  NsrR repressor fliAp2 Sigma28 -218.0 -237.5 fliA, fliZ, tcyJ
caaattcaatAAATTGCAATTcaacttgtag
2002021 2002032 [GEA], [HIBSCS] [5]
  NsrR repressor fliAp2 Sigma28 -5.0 -24.5 fliA, fliZ, tcyJ
gccctgcgttATATGAGTTATcggcatgatt
2001808 2001819 [GEA], [HIBSCS] [5]
  NsrR repressor grxD Sigma70 -13.0 -74.5 grxD
ggcatcggaaAATAACATTTTcatcacgctt
1734170 1734181 [GEA], [HIBSCS] [5]
  NsrR repressor hcpp nd 6.0 -26.0 hcp, hcr, poxB
accttttaaaGTTATATTTAATATACATGtttaaggtta
913831 913849 [BCE], [GEA], [HIBSCS], [SM] [2], [5], [8]
  NsrR repressor hmpAp Sigma38 -38.0 -75.5 hmp
aaaacaccaaAGAACCATTTAcattgcaggg
2685754 2685765 [GEA], [HIBSCS] [5]
  NsrR repressor hmpAp Sigma38 2.0 -37.0 hmp
tttttataagATGCATTTGAGATACATCAattaagatgc
2685789 2685807 [AIBSCS], [GEA] [1]
  NsrR repressor hmpAp Sigma38 20.0 -18.5 hmp
tacatcaattAAGATGCAAAAaaaggaagac
2685811 2685822 [GEA], [HIBSCS] [5]
  NsrR repressor hycAp Sigma54 -70.0 -96.5 hycA, hycB, hycC, hycD, hycE, hycF, hycG, hycH, hycI
cacggcgacgAAATTCATCTTtagcttaaaa
2850526 2850537 [GEA], [HIBSCS] [5]
  NsrR repressor hypAp Sigma54 -96.0 -115.5 hypA, hypB, hypC, hypD, hypE, fhlA
ttttaagctaAAGATGAATTTcgtcgccgtg
2850526 2850537 [GEA], [HIBSCS] [5]
  NsrR repressor lrpp Sigma70 52.0 -215.5 lrp
catgcatgtaAATACCATGTTtaccgtgcta
932374 932385 [GEA], [HIBSCS] [5]
  NsrR repressor mepHp Sigma70 -61.0 -138.5 mepH
tagctttcacTGCTGCATTTTtttgcgctcg
1734291 1734302 [GEA], [HIBSCS] [5]
  NsrR repressor mhpTp Sigma32 -484.0 -556.5 mhpT
actgccgagaACGTGCATTTTgtatgcccat
374897 374908 [GEA], [HIBSCS] [5]
  NsrR repressor ndhp Sigma70 6.0 -87.5 ndh
ctcaatagcgAAGAACATTTTcattgctgta
1165992 1166003 [GEA], [HIBSCS] [5]
  NsrR repressor norRp nd 21.0 1.5 norR
atcaacggaaAAACTCATCTTtgcctcactg
2832282 2832293 [GEA], [HIBSCS] [5]
  NsrR repressor nrfAp Sigma70 -121.0 -213.5 nrfA, nrfB, nrfC, nrfD, nrfE, nrfF, nrfG
ttctttgaggAACATGCAGTTatgcatgctg
4287545 4287556 [GEA], [HIBSCS] [5], [8]
  NsrR repressor nrfAp Sigma70 -63.0 -156.0 nrfA, nrfB, nrfC, nrfD, nrfE, nrfF, nrfG
taactctaaaGTGGTATTTTACATGCACTtacaattgat
4287599 4287617 [BCE], [GEA], [HIBSCS], [SM] [5], [9]
  NsrR repressor pgpCp Sigma32 131.0 41.5 pgpC, tadA
gctgatgcaaTGTTCCATCTAagtcaaaaaa
2698503 2698514 [GEA], [HIBSCS] [5]
  NsrR repressor rfep Sigma70 -1.0 -116.5 rfe, wzzE, wecB, wecC, rffG, rffH, rffC, wecE, wzxE, rffT, wzyE, rffM
catgttatgcAATTTGCATATcaaatggtta
3967794 3967805 [GEA], [HIBSCS] [5]
  NsrR repressor rybBp Sigma24 nd 888057.0 rybB nd nd [GEA] [10]
  NsrR repressor sodBp Sigma70 -37.0 -91.5 sodB
gcaacagggtAAGTTCATCTTttgtctcacc
1735281 1735292 [AIBSCS], [GEA] [5]
  NsrR repressor sufAp Sigma70 -68.0 -100.5 sufA, sufB, sufC, sufD, sufS, sufE
tttaccgtaaAACATGCTTTTtgcctgcttt
1764481 1764492 [GEA], [HIBSCS] [5], [11]
  NsrR repressor sufAp Sigma70 -6.0 -38.5 sufA, sufB, sufC, sufD, sufS, sufE
ttcagcgtatAACAGCATGTTagtgataatg
1764419 1764430 [GEA], [HIBSCS] [5], [11]
  NsrR repressor tehAp nd -1.0 -38.0 tehA, tehB
aattccataaAATGCATTTCAAATATACTttataaatta
1500526 1500544 [AIBSCS], [GEA], [HIBSCS] [1], [5]
  NsrR repressor tehAp nd 28.0 -9.5 tehA, tehB
taaattaaacAAAATGAGTAAgaagatgcag
1500558 1500569 [GEA], [HIBSCS] [5]
  NsrR repressor thrSp nd 80.0 -84.5 thrS, infC, rpmI, rplT, pheM, pheS, pheT, ihfA
agttcattgcGAAACCATCTAgccaacaaat
1802649 1802660 [GEA], [HIBSCS] [5]
  NsrR repressor tsgAp nd -64.0 -112.5 tsgA
atcacctcttAAAATGCAATTtagcaaccga
3492450 3492461 [GEA], [HIBSCS] [5]
  NsrR repressor ydbDp Sigma38 39.0 -39.5 ydbD
acaaaagggaAAGATGCATTTcccttttttt
1475099 1475110 [GEA], [HIBSCS] [5]
  NsrR repressor yeaEp Sigma70 5.0 -84.5 yeaE
atgccctggaAAGATGCATTAtcagaatttg
1865715 1865726 [GEA], [HIBSCS] [5]
  NsrR repressor yeaRp Sigma70 -32.0 -78.0 yeaR, yoaG
cgcctgataaTTTGCATTTTAAATACCATttattggtta
1880017 1880035 [AIBSCS], [GEA] [4]
  NsrR repressor ygbAp nd -118.0 -140.5 ygbA
aaagctgcaaAACAGCATCTTtcccggaacc
2856941 2856952 [GEA], [HIBSCS] [5]
  NsrR repressor ygbAp nd -7.0 -29.0 ygbA
acctcattaaGATGTATTTATATTACATCttaatcttaa
2856826 2856844 [AIBSCS], [GEA], [HIBSCS] [1], [5]
  NsrR repressor ygbAp nd -1.0 -23.5 ygbA
ccacctcattAAGATGTATTTatattacatc
2856824 2856835 [GEA], [HIBSCS] [5]
  NsrR repressor yibDp1 Sigma70 -115.0 -183.5 waaH
actgacaggaTTTTACATATTtaacagatta
3790259 3790270 [GEA], [HIBSCS] [5]
  NsrR repressor ytfEp nd -12.0 -38.0 ytfE
aataagataaGATGTATTTTAAATGCATCtttaaggcaa
4432012 4432030 [AIBSCS], [GEA], [HIBSCS], [SM] [1], [5], [8]


Alignment and PSSM for NsrR TFBSs    

Aligned TFBS of NsrR   
  Sequence
  AGAAGATGTTGTAA
  GTAAAATGCAGAGG
  AAAAGAGGCATATT
  AGAACGTGCATTTT
  TAAACATGTATATT
  TAAACATGGTATTT
  TGAAAATGTTCTTC
  GTGAAATGTATTTT
  GAAAGATGCATTTC
  ATAAAATGCATTTC
  ACAAAATGAGTAAG
  TGAAAATGTTATTT
  AAAAAATGCAGCAG
  AAAAGATGAACTTA
  CTAACATGCTGTTA
  AAAACATGCTTTTT
  GCTAGATGGTTTCG
  GAAAGATGCATTAT
  TTAAAATGCAAATT
  GTTATATGAGTTAT
  ATAAATTGCAATTC
  ATTACATGATTATG
  TTTAGATGTAAATC
  TGTAAATGGTTCTT
  ATAAGATGCATTTG
  TTAAGATGCAAAAA
  CTTAGATGGAACAT
  GTAATATGCCGATG
  CAAAGATGAGTTTT
  TAAAGATGAATTTC
  TTAAGATGTATTTA
  GAAAGATGCTGTTT
  TTAAAATGCAATTT
  TAAATATGTAAAAT
  TTGATATGCAAATT
  GGAACATGCAGTTA
  TTTACATGCACTTA
  TAAAGATGCATTTA
  GTAACATGCATTAC

Position weight matrix (PWM).   
A	11	13	30	39	11	37	0	0	6	25	10	11	9	8
C	3	2	0	0	9	0	0	0	21	1	3	3	1	7
G	10	6	2	0	15	1	1	39	4	3	7	0	1	7
T	15	18	7	0	4	1	38	0	8	10	19	25	28	17

PWM logo   


 


Evolutionary conservation of regulatory elements    
     Note: Evolutionary conservation of regulatory interactions and promoters is limited to gammaproteobacteria.
TF-target gene evolutionary conservation
Promoter-target gene evolutionary conservation


Evidence    

 [APPHINH] Assay of protein purified to homogeneity from its native host

 [HIFS] Human inference of function from sequence

 [IEP] Inferred from expression pattern

 [IPI] Inferred from physical interaction

 [BPP] Binding of purified proteins

 [GEA] Gene expression analysis

 [HIBSCS] Human inference based on similarity to consensus sequences

 [SM] Site mutation

 [BCE] Binding of cellular extracts

 [AIBSCS] Automated inference based on similarity to consensus sequences



Reference(s)    

 [1] Bodenmiller DM., Spiro S., 2006, The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator., J Bacteriol 188(3):874-81

 [2] Chismon DL., Browning DF., Farrant GK., Busby SJ., 2010, Unusual organization, complexity and redundancy at the Escherichia coli hcp-hcr operon promoter., Biochem J 430(1):61-8

 [3] Efromovich S., Grainger D., Bodenmiller D., Spiro S., 2008, Genome-wide identification of binding sites for the nitric oxide-sensitive transcriptional regulator NsrR., Methods Enzymol 437:211-33

 [4] Lin HY., Bledsoe PJ., Stewart V., 2007, Activation of yeaR-yoaG operon transcription by the nitrate-responsive regulator NarL is independent of oxygen- responsive regulator Fnr in Escherichia coli K-12., J Bacteriol 189(21):7539-48

 [5] Partridge JD., Bodenmiller DM., Humphrys MS., Spiro S., 2009, NsrR targets in the Escherichia coli genome: new insights into DNA sequence requirements for binding and a role for NsrR in the regulation of motility., Mol Microbiol 73(4):680-94

 [6] Tucker NP., Hicks MG., Clarke TA., Crack JC., Chandra G., Le Brun NE., Dixon R., Hutchings MI., 2008, The transcriptional repressor protein NsrR senses nitric oxide directly via a [2Fe-2S] cluster., PLoS ONE 3(11):e3623

 [7] Rankin LD., Bodenmiller DM., Partridge JD., Nishino SF., Spain JC., Spiro S., 2008, Escherichia coli NsrR regulates a pathway for the oxidation of 3-nitrotyramine to 4-hydroxy-3-nitrophenylacetate., J Bacteriol 190(18):6170-7

 [8] Filenko N., Spiro S., Browning DF., Squire D., Overton TW., Cole J., Constantinidou C., 2007, The NsrR regulon of Escherichia coli K-12 includes genes encoding the hybrid cluster protein and the periplasmic, respiratory nitrite reductase., J Bacteriol 189(12):4410-7

 [9] Browning DF., Lee DJ., Spiro S., Busby SJ., 2010, Down-regulation of the Escherichia coli K-12 nrf promoter by binding of the NsrR nitric oxide-sensing transcription repressor to an upstream site., J Bacteriol 192(14):3824-8

 [10] Thompson KM., Rhodius VA., Gottesman S., 2007, {sigma}E Regulates and Is Regulated by a Small RNA in Escherichia coli., J Bacteriol 189(11):4243-56

 [11] Chhabra S., Spiro S., 2015, Inefficient translation of nsrR constrains behaviour of the NsrR regulon in Escherichia coli., Microbiology 161(10):2029-38

 [12] Schwartz CJ., Giel JL., Patschkowski T., Luther C., Ruzicka FJ., Beinert H., Kiley PJ., 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 U S A 98(26):14895-900

 [13] Rodionov DA., Dubchak IL., Arkin AP., Alm EJ., Gelfand MS., 2005, Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks., PLoS Comput Biol 1(5):e55

 [14] Cairrao F., Cruz A., Mori H., Arraiano CM., 2003, Cold shock induction of RNase R and its role in the maturation of the quality control mediator SsrA/tmRNA., Mol Microbiol 50(4):1349-60

 [15] Lovgren JM., Wikstrom PM., 2001, The rlmB gene is essential for formation of Gm2251 in 23S rRNA but not for ribosome maturation in Escherichia coli., J Bacteriol 183(23):6957-60



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