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SoxS DNA-binding transcriptional dual regulator

Synonyms: SoxS
Summary:
SoxS is a dual transcriptional activator and participates in the removal of superoxide and nitric oxide and protection from organic solvents and antibiotics [1, 5, 30, 34] SoxS shares 49% identity with MarA and the N-terminal domain of Rob [35] These proteins activate a common set of about 50 target genes [8, 12] the marA/soxS/rob regulon, involved in antibiotic resistance [19, 36] superoxide resistance [34, 37] and tolerance to organic solvents []and heavy metals [] The activity of each protein is induced by different signals: the activity of Rob is increased with dipyridyl, bile salts, or decanoate [38] and the activities of MarA and SoxS are increased by the aromatic weak acid salicylate [12]CITS:[27098660]|and by oxidative stress [] respectively.
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Transcription factor      
TF conformation(s):
Name Conformation Type TF-Effector Interaction Type Apo/Holo Conformation Evidence (Confirmed, Strong, Weak) References
SoxS Functional   [IE] [1], [2], [3], [4], [5], [6], [7]
Evolutionary Family: AraC/XylS
Connectivity class: Local Regulator
Gene name: soxS
  Genome position: 4277060-4277383
  Length: 324 bp / 107 aa
Operon name: soxS
TU(s) encoding the TF:
Transcription unit        Promoter
soxS
soxSp


Regulon       
Regulated gene(s) acnA, acrA, acrB, acrZ, aldA, decR, fldA, fldB, fpr, fumC, fur, inaA, lpxC, marA, marB, marR, micF, nepI, nfo, nfsA, nfsB, ompN, pgi, poxB, pqiA, pqiB, pqiC, ptsG, ribA, rimK, rob, sodA, soxS, tolC, uof, waaY, waaZ, ybjC, ybjN, ydbK, ygiA, ygiB, ygiC, yrbL, zinT, zwf
Multifun term(s) of regulated gene(s) MultiFun Term (List of genes associated to the multifun term)
membrane (8)
drug resistance/sensitivity (7)
Transcription related (6)
activator (5)
repressor (5)
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Regulated operon(s) acnA, acrAB, acrZ, aldA, decR, fldA-uof-fur, fldB, fpr, fumAC, hcp-hcr-poxB-ltaE-ybjT, inaA, marRAB, micF, mraZ-rsmH-ftsLI-murEF-mraY-murD-ftsW-murGC-ddlB-ftsQAZ-lpxC, nepI, nfo, nfsB, pgi, pqiABC, ptsG, ribA, rirA-waaQGPSBOJYZU, rob, sodA, soxS, tolC-ygiABC, ybjC-nfsA-rimK-ybjN, ydbK-ompN, yrbL, zinT, zwf
First gene in the operon(s) acnA, acrA, acrZ, aldA, decR, fldA, fldB, fpr, fumC, inaA, lpxC, marR, micF, nepI, nfo, nfsB, pgi, poxB, pqiA, ptsG, ribA, rob, sodA, soxS, tolC, tolC, uof, waaY, ybjC, ydbK, ydbK, yrbL, zinT, zwf
Simple and complex regulons AcrR,CRP,CpxR,Cra,Fis,MarA,MarR,Rob,SoxS
AcrR,EnvR,MarA,MprA,PhoP,Rob,SoxS
AcrR,FNR,Fur,SoxR,SoxS
AcrR,H-NS,HU,IHF,Lrp,MarA,OmpR,Rob,SoxS
ArcA,CRP,Cra,FNR,MarA,Rob,SoxS
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Simple and complex regulatory phrases Regulatory phrase (List of promoters regulated by the phrase)
[SoxS,-](1)
[SoxS,+](26)


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
  SoxS activator acnAp2 Sigma70 -51.5 nd acnA 1335734 1335747 [CHIP-SV], [MSI] nd
  SoxS activator acnAp2 Sigma70 -51.5 nd acnA 1335734 1335747 [CHIP-SV], [MSI] nd
  SoxS activator acnAp2 Sigma70 -51.5 -101.0 acnA
aaggtttctcCTCTTTTATCAATTTGGGTTgttatcaaat
1335720 1335740 [BPP], [GEA], [HIBSCS] [8], [9]
  SoxS activator acrAp Sigma70 -72.5 nd acrA, acrB 485616 485636 [CHIP-SV], [MSI] nd
  SoxS activator acrAp Sigma70 -72.5 -151.5 acrA, acrB
tcacgaacatATGGCACGAAAAACCAAACAagaagcgcaa
485761 485780 [BPP], [GEA], [HIBSCS] [9], [10]
  SoxS activator acrAp Sigma70 -72.5 nd acrA, acrB 485616 485636 [CHIP-SV], [MSI] nd
  SoxS activator acrZp Sigma70 -40.5 -62.5 acrZ
cgcaaagctgACCGCACAAAAGGGGAGTGCttttctgtgc
794701 794720 [GEA], [IHBCE] [11]
  SoxS activator aldAp Sigma70 -161.0 -203.5 aldA
gcgatggaaaGTCGCTCGTTACGTTAAAAAttgcccgttt
1488019 1488038 [AIBSCS], [GEA] [8]
  SoxS activator fldAp nd -61.5 nd fldA, uof, fur 711450 711470 [CHIP-SV], [MSI] nd
  SoxS activator fldAp nd -61.5 nd fldA, uof, fur 711450 711470 [CHIP-SV], [MSI] nd
  SoxS activator fldAp nd -61.5 -117.5 fldA, uof, fur
aaacgagcagGACTGCACACTGTGCTACATgaaagtggaa
711573 711592 [BPP], [GEA], [HIBSCS] [10], [12], [13]
  SoxS activator fldBp Sigma70 -49.0 -82.5 fldB
ttatggtcacTCATTTGATCCATTATGCCTtattgtgccg
3039763 3039782 [GEA], [HIBSCS] [14]
  SoxS activator fldBp Sigma70 -38.0 -71.0 fldB
catttgatccATTATGCCTTATTGTGCCGTgactaaagcg
3039774 3039794 [GEA], [HIBSCS] [8], [14]
  SoxS activator fprp Sigma70 -56.5 -83.5 fpr
cgaaggactgGAAGGCTCAATCGATCAAATcaatcagagg
4114546 4114565 [BPP], [GEA], [HIBSCS] [9], [10], [12], [15]
  SoxS activator fprp Sigma70 -56.5 nd fpr 4114433 4114453 [CHIP-SV], [MSI] nd
  SoxS activator fprp Sigma70 -56.5 nd fpr 4114433 4114453 [CHIP-SV], [MSI] nd
  SoxS activator fumCp Sigma38 19.5 -102.5 fumC
gataacaaatGTTTGGTCTTTCGTGCCATGtaaaaaaacc
1686681 1686700 [BPP], [CHIP-SV], [GEA], [MSI] [12], [15], [16], [17],



High-throughput Transcription factor binding sites (TFBSs)
      

  Functional conformation Function Object name Object type Distance to first Gene Sequence LeftPos RightPos Evidence (Confirmed, Strong, Weak) References
  SoxS activator yhbW nd nd 3303372 3303391 [ICWHO] nd
  SoxS activator map-glnD-dapD nd nd 189597 189616 [ICWHO] nd
  SoxS activator mdaB nd nd 3172452 3172471 [ICWHO] nd
Other High-throughput regulatory interactions with weak evidence


Alignment and PSSM for SoxS TFBSs    

Position weight matrix (PWM).   
A	7	3	2	12	9	1	10	11	8	5	7	6	3	0	0	4	11	1
C	2	1	0	1	5	15	9	2	1	3	6	1	0	1	22	15	2	7
G	1	3	1	11	10	3	5	6	0	1	0	17	1	26	1	3	9	0
T	17	20	24	3	3	8	3	8	18	18	14	3	23	0	4	5	5	19

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    

 [IE] Inferred from experiment

 [CHIP-SV] ChIP analysis and statistical validation of TFBSs

 [MSI] Mapping of signal intensities

 [BPP] Binding of purified proteins

 [GEA] Gene expression analysis

 [HIBSCS] Human inference based on similarity to consensus sequences

 [IHBCE] Inferred by a human based on computational evidence

 [AIBSCS] Automated inference based on similarity to consensus sequences

 [ICWHO] Inferred computationally without human oversight



Reference(s)    

 [1] Amabile-Cuevas CF., Demple B., 1991, Molecular characterization of the soxRS genes of Escherichia coli: two genes control a superoxide stress regulon., Nucleic Acids Res 19(16):4479-84

 [2] Blattner FR., Burland V., Plunkett G., Sofia HJ., Daniels DL., 1993, Analysis of the Escherichia coli genome. IV. DNA sequence of the region from 89.2 to 92.8 minutes., Nucleic Acids Res 21(23):5408-17

 [3] Fawcett WP., Wolf RE., 1994, Purification of a MalE-SoxS fusion protein and identification of the control sites of Escherichia coli superoxide-inducible genes., Mol Microbiol 14(4):669-79

 [4] Fawcett WP., Wolf RE., 1995, Genetic definition of the Escherichia coli zwf "soxbox," the DNA binding site for SoxS-mediated induction of glucose 6-phosphate dehydrogenase in response to superoxide., J Bacteriol 177(7):1742-50

 [5] Li Z., Demple B., 1994, SoxS, an activator of superoxide stress genes in Escherichia coli. Purification and interaction with DNA., J Biol Chem 269(28):18371-7

 [6] Nunoshiba T., Hidalgo E., Li Z., Demple B., 1993, Negative autoregulation by the Escherichia coli SoxS protein: a dampening mechanism for the soxRS redox stress response., J Bacteriol 175(22):7492-4

 [7] Wu J., Weiss B., 1991, Two divergently transcribed genes, soxR and soxS, control a superoxide response regulon of Escherichia coli., J Bacteriol 173(9):2864-71

 [8] Martin RG., Rosner JL., 2002, Genomics of the marA/soxS/rob regulon of Escherichia coli: identification of directly activated promoters by application of molecular genetics and informatics to microarray data., Mol Microbiol 44(6):1611-24

 [9] Martin RG., Rosner JL., 2011, Promoter discrimination at class I MarA regulon promoters mediated by glutamic acid 89 of the MarA transcriptional activator of Escherichia coli., J Bacteriol 193(2):506-15

 [10] Martin RG., Gillette WK., Rhee S., Rosner JL., 1999, Structural requirements for marbox function in transcriptional activation of mar/sox/rob regulon promoters in Escherichia coli: sequence, orientation and spatial relationship to the core promoter., Mol Microbiol 34(3):431-41

 [11] Hobbs EC., Yin X., Paul BJ., Astarita JL., Storz G., 2012, Conserved small protein associates with the multidrug efflux pump AcrB and differentially affects antibiotic resistance., Proc Natl Acad Sci U S A 109(41):16696-701

 [12] Pomposiello PJ., Bennik MH., Demple B., 2001, Genome-wide transcriptional profiling of the Escherichia coli responses to superoxide stress and sodium salicylate., J Bacteriol 183(13):3890-902

 [13] Zheng M., Doan B., Schneider TD., Storz G., 1999, OxyR and SoxRS regulation of fur., J Bacteriol 181(15):4639-43

 [14] Gaudu P., Weiss B., 2000, Flavodoxin mutants of Escherichia coli K-12., J Bacteriol 182(7):1788-93

 [15] Jair KW., Martin RG., Rosner JL., Fujita N., Ishihama A., Wolf RE., 1995, Purification and regulatory properties of MarA protein, a transcriptional activator of Escherichia coli multiple antibiotic and superoxide resistance promoters., J Bacteriol 177(24):7100-4

 [16] Benov L., Fridovich I., 2002, Induction of the soxRS regulon of Escherichia coli by glycolaldehyde., Arch Biochem Biophys 407(1):45-8

 [17] Park SJ., Gunsalus RP., 1995, Oxygen, iron, carbon, and superoxide control of the fumarase fumA and fumC genes of Escherichia coli: role of the arcA, fnr, and soxR gene products., J Bacteriol 177(21):6255-62

 [18] null, null, null, null

 [19] Martin RG., Jair KW., Wolf RE., Rosner JL., 1996, Autoactivation of the marRAB multiple antibiotic resistance operon by the MarA transcriptional activator in Escherichia coli., J Bacteriol 178(8):2216-23

 [20] Delihas N., Forst S., 2001, MicF: an antisense RNA gene involved in response of Escherichia coli to global stress factors., J Mol Biol 313(1):1-12

 [21] Jair KW., Fawcett WP., Fujita N., Ishihama A., Wolf RE., 1996, Ambidextrous transcriptional activation by SoxS: requirement for the C-terminal domain of the RNA polymerase alpha subunit in a subset of Escherichia coli superoxide-inducible genes., Mol Microbiol 19(2):307-17

 [22] Rungrassamee W., Liu X., Pomposiello PJ., 2008, Activation of glucose transport under oxidative stress in Escherichia coli., Arch Microbiol 190(1):41-9

 [23] Koh YS., Roe JH., 1996, Dual regulation of the paraquat-inducible gene pqi-5 by SoxS and RpoS in Escherichia coli., Mol Microbiol 22(1):53-61

 [24] Koh YS., Choih J., Lee JH., Roe JH., 1996, Regulation of the ribA gene encoding GTP cyclohydrolase II by the soxRS locus in Escherichia coli., Mol Gen Genet 251(5):591-8

 [25] Koh YS., Chung WH., Lee JH., Roe JH., 1999, The reversed SoxS-binding site upstream of the ribA promoter in Escherichia coli., Mol Gen Genet 261(2):374-80

 [26] Schneiders T., Levy SB., 2006, MarA mediated transcriptional repression of the rob promoter., J Biol Chem 281(15):10049-51

 [27] Aono R., Tsukagoshi N., Yamamoto M., 1998, Involvement of outer membrane protein TolC, a possible member of the mar-sox regulon, in maintenance and improvement of organic solvent tolerance of Escherichia coli K-12., J Bacteriol 180(4):938-44

 [28] Rodionov DA., Gelfand MS., Mironov AA., Rakhmaninova AB., 2001, Comparative approach to analysis of regulation in complete genomes: multidrug resistance systems in gamma-proteobacteria., J Mol Microbiol Biotechnol 3(2):319-24

 [29] Zhang A., Rosner JL., Martin RG., 2008, Transcriptional activation by MarA, SoxS and Rob of two tolC promoters using one binding site: a complex promoter configuration for tolC in Escherichia coli., Mol Microbiol 69(6):1450-5

 [30] Lee JH., Lee KL., Yeo WS., Park SJ., Roe JH., 2009, SoxRS-mediated lipopolysaccharide modification enhances resistance against multiple drugs in Escherichia coli., J Bacteriol 191(13):4441-50

 [31] Paterson ES., Boucher SE., Lambert IB., 2002, Regulation of the nfsA Gene in Escherichia coli by SoxS., J Bacteriol 184(1):51-8

 [32] Nakayama T., Yonekura S., Yonei S., Zhang-Akiyama QM., 2013, Escherichia coli pyruvate:flavodoxin oxidoreductase, YdbK - regulation of expression and biological roles in protection against oxidative stress., Genes Genet Syst 88(3):175-88

 [33] Puskarova A., Ferianc P., Kormanec J., Homerova D., Farewell A., Nystrom T., 2002, Regulation of yodA encoding a novel cadmium-induced protein in Escherichia coli., Microbiology 148(Pt 12):3801-11

 [34] Nunoshiba T., Hidalgo E., Amabile Cuevas CF., Demple B., 1992, Two-stage control of an oxidative stress regulon: the Escherichia coli SoxR protein triggers redox-inducible expression of the soxS regulatory gene., J Bacteriol 174(19):6054-60

 [35] Cohen SP., Hachler H., Levy SB., 1993, Genetic and functional analysis of the multiple antibiotic resistance (mar) locus in Escherichia coli., J Bacteriol 175(5):1484-92

 [36] Ariza RR., Li Z., Ringstad N., Demple B., 1995, Activation of multiple antibiotic resistance and binding of stress-inducible promoters by Escherichia coli Rob protein., J Bacteriol 177(7):1655-61

 [37] Jair KW., Yu X., Skarstad K., Thony B., Fujita N., Ishihama A., Wolf RE., 1996, Transcriptional activation of promoters of the superoxide and multiple antibiotic resistance regulons by Rob, a binding protein of the Escherichia coli origin of chromosomal replication., J Bacteriol 178(9):2507-13

 [38] Rosenberg EY., Bertenthal D., Nilles ML., Bertrand KP., Nikaido H., 2003, Bile salts and fatty acids induce the expression of Escherichia coli AcrAB multidrug efflux pump through their interaction with Rob regulatory protein., Mol Microbiol 48(6):1609-19

 [39] Pomposiello PJ., Koutsolioutsou A., Carrasco D., Demple B., 2003, SoxRS-regulated expression and genetic analysis of the yggX gene of Escherichia coli., J Bacteriol 185(22):6624-32

 [40] Wood TI., Griffith KL., Fawcett WP., Jair KW., Schneider TD., Wolf RE., 1999, Interdependence of the position and orientation of SoxS binding sites in the transcriptional activation of the class I subset of Escherichia coli superoxide-inducible promoters., Mol Microbiol 34(3):414-30

 [41] Kwon HJ., Bennik MH., Demple B., Ellenberger T., 2000, Crystal structure of the Escherichia coli Rob transcription factor in complex with DNA., Nat Struct Biol 7(5):424-30

 [42] Dangi B., Pelupessey P., Martin RG., Rosner JL., Louis JM., Gronenborn AM., 2001, Structure and dynamics of MarA-DNA complexes: an NMR investigation., J Mol Biol 314(1):113-27

 [43] Griffith KL., Wolf RE., 2001, Systematic mutagenesis of the DNA binding sites for SoxS in the Escherichia coli zwf and fpr promoters: identifying nucleotides required for DNA binding and transcription activation., Mol Microbiol 40(5):1141-54

 [44] Zafar MA., Shah IM., Wolf RE., 2010, Protein-protein interactions between sigma(70) region 4 of RNA polymerase and Escherichia coli SoxS, a transcription activator that functions by the prerecruitment mechanism: evidence for "off-DNA" and "on-DNA" interactions., J Mol Biol 401(1):13-32

 [45] Gallegos MT., Schleif R., Bairoch A., Hofmann K., Ramos JL., 1997, Arac/XylS family of transcriptional regulators., Microbiol Mol Biol Rev 61(4):393-410

 [46] Griffith KL., Wolf RE., 2002, A comprehensive alanine scanning mutagenesis of the Escherichia coli transcriptional activator SoxS: identifying amino acids important for DNA binding and transcription activation., J Mol Biol 322(2):237-57

 [47] Graham AI., Sanguinetti G., Bramall N., McLeod CW., Poole RK., 2012, Dynamics of a starvation-to-surfeit shift: a transcriptomic and modelling analysis of the bacterial response to zinc reveals transient behaviour of the Fur and SoxS regulators., Microbiology 158(Pt 1):284-92



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