RegulonDB RegulonDB 11.1: Operon Form
   

rrsA-ileT-alaT-rrlA-rrfA operon and associated TUs in Escherichia coli K-12 genome




Operon      
Name: rrsA-ileT-alaT-rrlA-rrfA
This page displays every known transcription unit of this operon and their known regulation.


Transcription unit          
Name: rrsA-ileT-alaT-rrlA-rrfA
Synonym(s): rrnA
Gene(s): rrsA, ileT, alaT, rrlA, rrfA   Genome Browser M3D Gene expression COLOMBOS
Note(s): The seven ribosomal operons of E. coli are complexly transcribed. Each operon has two σ70 promoters (p1 and p2); their transcription starts with a large precursor that contains rRNAs Gralla JD.,2005; they are the target of regulation by the alarmone ppGpp, several triphosphate nucleotides (NTPs), and the transcriptional regulators FIS and HNS. FIS and HNS regulate at the p1; however, ppGpp and NTPs control both promoters in accordance with their concentration changes, even in the absence of the transcriptional regulators Paul BJ,2004. Schneider DA,2003. Zhang X,2002. In addition, these two small regulating metabolites (ppGpp and NTPs) require the help of the DskA coregulatory protein that binds to the RNA polymerase Paul BJ,2004.
The net amount of rRNA transcription can be seen as a complex function of the ratio of inhibitors to activators. HNS/Fis and ppGpp/NTP ratios are the highest ones during slow growth and the lowest ones during rapid growth; the ribosomal production is in accordance to the growth rate (higher in rapid growth and lower in slow growth) Gralla JD.,2005. Schneider DA,2003.
It is important to note that the ribosomal gene-containing operons also encode genes whose products interact with the RNA polymerase and participate in the translation elongation and in the replication apparatus.
Reviews: Dennis PP, Ehrenberg M, Bremer H,2004. Condon C, Squires C, Squires CL,1995. Zengel JM, Lindahl L,1994. Lindahl L, Zengel JM,1986. Gralla JD.,2005. Paul BJ,2004. Additional reference:Keener J. and Nomura M. (1996). Regulation of Ribosome Synthesis, in: Neidhardt, F. (Editor in Chief) et al., E. coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, D.C., p.1417-1431.
Evidence: [EXP-IDA-BOUNDARIES-DEFINED] Boundaries of transcription experimentally identified
Reference(s): [1] Gralla JD. 2005
[2] Paul BJ., et al., 2004
[3] Schneider DA., et al., 2003
[4] Zhang X., et al., 2002
Promoter
Name: rrsAp1
+1: 4035239
Sigma Factor: Sigma70 Sigmulon
Distance from start of the gene: 292
Sequence: cagaaaattattttaaatttcctcttgtcaggccggaataactccctataatgcgccaccActgacacggaacaacggcaa
                         -35                   -10          +1                   
Note(s): Keener J. and Nomura M. (1996). Regulation of Ribosome Synthesis, in: Neidhardt, F. (Editor in Chief) et al., E. coli and Salmonella. Cellular and Molecular Biology. ASM Press, Washington, D.C., p. 1417-1431.
Although the organization and sequence of the seven major ribosomal RNA (rRNA) P1 promoters are highly conserved, the upstream region differs considerably in its regulation, with different transcription factor affinities for the individual upstream regions and strikingly different architectures of the resulting DNA-protein complexes that form with the individual rRNA operon upstream regions Hillebrand A, Wurm R, Menzel A, Wagner R,2005
Based on studies of binding sites determined using gel shift and footprinting analyses with Lrp and H-NS regulator proteins, it was demonstrated that both proteins interact with obvious synergism in the repression of all seven E. coli rrn P1 promoter upstream regions; as a result, they help the efficient shutdown of rRNA synthesis. Likewise, both proteins could be a transient heteromer via a protein-protein interaction that interferes with the RNA polymerase, and this way it may alter the DNA of the upstream regions of all seven ribosomal P1 promoters Pul U,2005.
The rrsAp1 is also recognized by σ32, which shows a -35 box, spacer, and -10 box, CGGAAT-14-CGCCAC, based on similarity to the consensus sequence of the set of known functional promoters for this σ factor, for which there is strong experimental evidence: high homology; score, 7.24; P-value, 2.35e05.
Evidence: [COMP-AINF]
[COMP-HINF-POSITIONAL-IDENTIFICATION]
Reference(s): [5] Huerta AM., et al., 2003
[6] Newlands JT., et al., 1993
TF binding sites (TFBSs)
[Fis,+] Phrase
Type Transcription factor Function Promoter Binding Sites Growth Conditions Evidence Confidence level (C: Confirmed, S: Strong, W: Weak) Reference(s)
LeftPos RightPos Central Rel-Pos Sequence
remote Fis activator rrsAp1 4035099 4035113 -133.0 gggagcaggtGGCGAATTTCGCCCGagaaatcgcc nd [EXP-IEP-GENE-EXPRESSION-ANALYSIS], [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] W [7]
remote Fis activator rrsAp1 4035121 4035135 -111.0 ccgagaaatcGCCCATTTAACCGACaaaccgacgc nd [EXP-IEP-GENE-EXPRESSION-ANALYSIS], [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] W [7]
proximal Fis activator rrsAp1 4035141 4035155 -91.0 ccgacaaaccGACGCTGAAATAAGCataaagaata nd [EXP-IEP-GENE-EXPRESSION-ANALYSIS], [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] W [7]
proximal Fis activator rrsAp1 4035161 4035175 -71.0 taagcataaaGAATAAAAAATGCGCggtcagaaaa nd [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] nd [7]
[Lrp,-] Phrase
Type Transcription factor Function Promoter Binding Sites Growth Conditions Evidence Confidence level (C: Confirmed, S: Strong, W: Weak) Reference(s)
LeftPos RightPos Central Rel-Pos Sequence
proximal Lrp-L-leucine repressor rrsAp1 4035160 4035171 -73.0 ataagcataaAGAATAAAAAATgcgcggtcag nd [EXP-IDA-BINDING-OF-CELLULAR-EXTRACTS] nd [8]
proximal Lrp-L-leucine repressor rrsAp1 4035180 4035191 -53.0 atgcgcggtcAGAAAATTATTTtaaatttcct nd [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] nd [8]
Allosteric regulation of RNA-polymerase
  Regulator Function Promoter target of RNApol Growth Conditions Note Evidence Reference
  DksA inhibition rrsAp1 nd   [EXP-IDA-PURIFIED-PROTEIN]
[EXP-IEP-GENE-EXPRESSION-ANALYSIS] 		[9]
  DksA-ppGpp inhibition rrsAp1 nd   [EXP-IDA-PURIFIED-PROTEIN]
[EXP-IEP-GENE-EXPRESSION-ANALYSIS]
[EXP-IMP] 		[9]
  ppGpp inhibition rrsAp1 nd   [EXP-IMP] [9]
Evidence: [EXP-IDA-PURIFIED-PROTEIN] Assay of protein purified to homogeneity
[EXP-IEP-GENE-EXPRESSION-ANALYSIS] Gene expression analysis
[EXP-IMP] Inferred from mutant phenotype
Reference(s): [9] Paul BJ., et al., 2004


Transcription unit          
Name: rrsA-ileT-alaT-rrlA-rrfA
Synonym(s): rrnA
Gene(s): rrsA, ileT, alaT, rrlA, rrfA   Genome Browser M3D Gene expression COLOMBOS
Note(s): The seven ribosomal operons of E. coli are complexly transcribed. Each operon has two σ70 promoters (p1 and p2); their transcription starts with a large precursor that contains rRNAs Gralla JD.,2005; they are the target of regulation by the alarmone ppGpp, several triphosphate nucleotides (NTPs), and the transcriptional regulators FIS and HNS. FIS and HNS regulate at the p1; however, ppGpp and NTPs control both promoters in accordance with their concentration changes, even in the absence of the transcriptional regulators Paul BJ,2004. Schneider DA,2003. Zhang X,2002. In addition, these two small regulating metabolites (ppGpp and NTPs) require the help of the DskA coregulatory protein that binds to the RNA polymerase Paul BJ,2004.
The net amount of rRNA transcription can be seen as a complex function of the ratio of inhibitors to activators. HNS/Fis and ppGpp/NTP ratios are the highest ones during slow growth and the lowest ones during rapid growth; the ribosomal production is in accordance to the growth rate (higher in rapid growth and lower in slow growth) Gralla JD.,2005. Schneider DA,2003.
It is important to note that the ribosomal gene-containing operons also encode genes whose products interact with the RNA polymerase and participate in the translation elongation and in the replication apparatus.
Reviews: Dennis PP, Ehrenberg M, Bremer H,2004. Condon C, Squires C, Squires CL,1995. Zengel JM, Lindahl L,1994. Lindahl L, Zengel JM,1986. Gralla JD.,2005. Paul BJ,2004. Additional reference:Keener J. and Nomura M. (1996). Regulation of Ribosome Synthesis, in: Neidhardt, F. (Editor in Chief) et al., E. coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, D.C., p.1417-1431.
Evidence: [EXP-IDA-BOUNDARIES-DEFINED] Boundaries of transcription experimentally identified
Reference(s): [1] Gralla JD. 2005
[2] Paul BJ., et al., 2004
[3] Schneider DA., et al., 2003
[4] Zhang X., et al., 2002
Promoter
Name: rrsAp
+1: 4035239
Sigma Factor: Sigma32 Sigmulon
Distance from start of the gene: 292
Sequence: cagaaaattattttaaatttcctcttgtcaggccggaataactccctataatgcgccaccActgacacggaacaacggcaa
                                  -35                 -10   +1                   
Note(s): Keener J. and Nomura M. (1996). Regulation of Ribosome Synthesis, in: Neidhardt, F. (Editor in Chief) et al., E. coli and Salmonella. Cellular and Molecular Biology. ASM Press, Washington, D.C., p. 1417-1431.
Although the organization and sequence of the seven major ribosomal RNA (rRNA) P1 promoters are highly conserved, the upstream region differs considerably in its regulation, with different transcription factor affinities for the individual upstream regions and strikingly different architectures of the resulting DNA-protein complexes that form with the individual rRNA operon upstream regions Hillebrand A, Wurm R, Menzel A, Wagner R,2005
Based on studies of binding sites determined using gel shift and footprinting analyses with Lrp and H-NS regulator proteins, it was demonstrated that both proteins interact with obvious synergism in the repression of all seven E. coli rrn P1 promoter upstream regions; as a result, they help the efficient shutdown of rRNA synthesis. Likewise, both proteins could be a transient heteromer via a protein-protein interaction that interferes with the RNA polymerase, and this way it may alter the DNA of the upstream regions of all seven ribosomal P1 promoters Pul U,2005.
The rrsAp1 is also recognized by σ32, which shows a -35 box, spacer, and -10 box, CGGAAT-14-CGCCAC, based on similarity to the consensus sequence of the set of known functional promoters for this σ factor, for which there is strong experimental evidence: high homology; score, 7.24; P-value, 2.35e05.
Evidence: [COMP-AINF]
[COMP-HINF-POSITIONAL-IDENTIFICATION]
Reference(s): [5] Huerta AM., et al., 2003
[6] Newlands JT., et al., 1993
TF binding sites (TFBSs)
[Fis,+] Phrase
Type Transcription factor Function Promoter Binding Sites Growth Conditions Evidence Confidence level (C: Confirmed, S: Strong, W: Weak) Reference(s)
LeftPos RightPos Central Rel-Pos Sequence
remote Fis activator rrsAp 4035099 4035113 -133.0 gggagcaggtGGCGAATTTCGCCCGagaaatcgcc nd [EXP-IEP-GENE-EXPRESSION-ANALYSIS], [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] W [7]
remote Fis activator rrsAp 4035121 4035135 -111.0 ccgagaaatcGCCCATTTAACCGACaaaccgacgc nd [EXP-IEP-GENE-EXPRESSION-ANALYSIS], [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] W [7]
proximal Fis activator rrsAp 4035141 4035155 -91.0 ccgacaaaccGACGCTGAAATAAGCataaagaata nd [EXP-IEP-GENE-EXPRESSION-ANALYSIS], [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] W [7]
proximal Fis activator rrsAp 4035161 4035175 -71.0 taagcataaaGAATAAAAAATGCGCggtcagaaaa nd [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] nd [7]
[Lrp,-] Phrase
Type Transcription factor Function Promoter Binding Sites Growth Conditions Evidence Confidence level (C: Confirmed, S: Strong, W: Weak) Reference(s)
LeftPos RightPos Central Rel-Pos Sequence
proximal Lrp-L-leucine repressor rrsAp 4035160 4035171 -73.0 ataagcataaAGAATAAAAAATgcgcggtcag nd [EXP-IDA-BINDING-OF-CELLULAR-EXTRACTS] nd [8]
proximal Lrp-L-leucine repressor rrsAp 4035180 4035191 -53.0 atgcgcggtcAGAAAATTATTTtaaatttcct nd [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] nd [8]
Allosteric regulation of RNA-polymerase
  Regulator Function Promoter target of RNApol Growth Conditions Note Evidence Reference
  DksA inhibition rrsAp nd   [EXP-IDA-PURIFIED-PROTEIN]
[EXP-IEP-GENE-EXPRESSION-ANALYSIS] 		[9]
  DksA-ppGpp inhibition rrsAp nd   [EXP-IDA-PURIFIED-PROTEIN]
[EXP-IEP-GENE-EXPRESSION-ANALYSIS]
[EXP-IMP] 		[9]
  ppGpp inhibition rrsAp nd   [EXP-IMP] [9]
Evidence: [EXP-IDA-PURIFIED-PROTEIN] Assay of protein purified to homogeneity
[EXP-IEP-GENE-EXPRESSION-ANALYSIS] Gene expression analysis
[EXP-IMP] Inferred from mutant phenotype
Reference(s): [9] Paul BJ., et al., 2004


Transcription unit       
Name: rrsA-ileT-alaT-rrlA-rrfA
Gene(s): rrsA, ileT, alaT, rrlA, rrfA   Genome Browser M3D Gene expression COLOMBOS
Note(s): The seven ribosomal operons of E. coli are complexly transcribed. Each operon has two σ70 promoters (p1 and p2); their transcription starts with a large precursor that contains rRNAs Gralla JD.,2005; they are the target of regulation by the alarmone ppGpp, several triphosphate nucleotides (NTPs), and the transcriptional regulators FIS and HNS. FIS and HNS regulate at the p1; however, ppGpp and NTPs control both promoters in accordance with their concentration changes, even in the absence of the transcriptional regulators Paul BJ,2004. Schneider DA,2003. Zhang X,2002. In addition, these two small regulating metabolites (ppGpp and NTPs) require the help of the DskA coregulatory protein that binds to the RNA polymerase Paul BJ,2004.
The net amount of rRNA transcription can be seen as a complex function of the ratio of inhibitors to activators. HNS/Fis and ppGpp/NTP ratios are the highest ones during slow growth and the lowest ones during rapid growth; the ribosomal production is in accordance to the growth rate (higher in rapid growth and lower in slow growth) Gralla JD.,2005. Schneider DA,2003.
It is important to note that the ribosomal gene-containing operons also encode genes whose products interact with the RNA polymerase and participate in the translation elongation and in the replication apparatus.
Reviews: Dennis PP, Ehrenberg M, Bremer H,2004. Condon C, Squires C, Squires CL,1995. Zengel JM, Lindahl L,1994. Lindahl L, Zengel JM,1986. Gralla JD.,2005. Paul BJ,2004. Additional reference:Keener J. and Nomura M. (1996). Regulation of Ribosome Synthesis, in: Neidhardt, F. (Editor in Chief) et al., E. coli and Salmonella: Cellular and Molecular Biology. ASM Press, Washington, D.C., p.1417-1431.
Promoter
Name: rrsAp2
+1: 4035356
Sigma Factor: Sigma70 Sigmulon
Distance from start of the gene: 175
Sequence: ccggcagagaaagcaaaaataaatgcttgactctgtagcgggaaggcgtattatgcacacCccgcgccgctgagaaaaagc
                           -35                   -10        +1                   
Evidence: [COMP-AINF]
[COMP-HINF-POSITIONAL-IDENTIFICATION]
[RS-EPT-CBR]
Reference(s): [5] Huerta AM., et al., 2003
[10] Salgado H, et al., 2012


Transcription unit       
Name: rrlA-rrfA
Gene(s): rrlA, rrfA   Genome Browser M3D Gene expression COLOMBOS
Note(s): A potential RNA G-quadruplex structure, formed by guanine-rich sequences located in the coding sequence region of the gene, was identified for rrlA. This structure could regulate the expression of the gene, as observed for hemL gene expression Shao X, Zhang W, Umar MI, Wong HY, Seng Z, Xie Y, Zhang Y, Yang L, Kwok CK, Deng X,2020.
Evidence: [IC-ADJ-GENES-SAME-BIO-PROCESS] Products of adjacent genes in the same biological process
Promoter
Name: rrlAp
+1: Unknown
Note(s): Zaslaver et al. demonstrated in 2006, by means of a library of fluorescent transcription fusions, that this promoter can be transcribed in vitro Zaslaver A,2006. Based on this, a putative promoter was suggested, but the +1 site of the transcription initiation has not been determined, although there exists promoter activity.
Evidence: [EXP-IEP]
Reference(s): [11] Zaslaver A., et al., 2006


Evidence    

 [COMP-AINF] Inferred computationally without human oversight

 [COMP-HINF-POSITIONAL-IDENTIFICATION] Human inference of promoter position

 [EXP-IEP-GENE-EXPRESSION-ANALYSIS] Gene expression analysis

 [EXP-IDA-BINDING-OF-PURIFIED-PROTEINS] Binding of purified proteins

 [EXP-IDA-BINDING-OF-CELLULAR-EXTRACTS] Binding of cellular extracts

 [RS-EPT-CBR] RNA-seq using two enrichment strategies for primary transcripts and consistent biological replicates

 [EXP-IEP] Inferred from expression pattern


Reference(s)    

 [1] Gralla JD., 2005, Escherichia coli ribosomal RNA transcription: regulatory roles for ppGpp, NTPs, architectural proteins and a polymerase-binding protein., Mol Microbiol 55(4):973-7

 [2] Paul BJ., Ross W., Gaal T., Gourse RL., 2004, rRNA transcription in Escherichia coli., Annu Rev Genet 38:749-70

 [3] Schneider DA., Gourse RL., 2003, Changes in Escherichia coli rRNA promoter activity correlate with changes in initiating nucleoside triphosphate and guanosine 5' diphosphate 3'-diphosphate concentrations after induction of feedback control of ribosome synthesis., J Bacteriol 185(20):6185-91

 [4] Zhang X., Dennis P., Ehrenberg M., Bremer H., 2002, Kinetic properties of rrn promoters in Escherichia coli., Biochimie 84(10):981-96

 [5] Huerta AM., Collado-Vides J., 2003, Sigma70 promoters in Escherichia coli: specific transcription in dense regions of overlapping promoter-like signals., J Mol Biol 333(2):261-78

 [6] Newlands JT., Gaal T., Mecsas J., Gourse RL., 1993, Transcription of the Escherichia coli rrnB P1 promoter by the heat shock RNA polymerase (E sigma 32) in vitro., J Bacteriol 175(3):661-8

 [7] Hirvonen CA., Ross W., Wozniak CE., Marasco E., Anthony JR., Aiyar SE., Newburn VH., Gourse RL., 2001, Contributions of UP elements and the transcription factor FIS to expression from the seven rrn P1 promoters in Escherichia coli., J Bacteriol 183(21):6305-14

 [8] Pul U., Wurm R., Lux B., Meltzer M., Menzel A., Wagner R., 2005, LRP and H-NS--cooperative partners for transcription regulation at Escherichia coli rRNA promoters., Mol Microbiol 58(3):864-76

 [9] Paul BJ., Barker MM., Ross W., Schneider DA., Webb C., Foster JW., Gourse RL., 2004, DksA: a critical component of the transcription initiation machinery that potentiates the regulation of rRNA promoters by ppGpp and the initiating NTP., Cell 118(3):311-22

 [10] Salgado H, Peralta-Gil M, Gama-Castro S, Santos-Zavaleta A, Muñiz-Rascado L, García-Sotelo JS, Weiss V, Solano-Lira H, Martínez-Flores I, Medina-Rivera A, Salgado-Osorio G, Alquicira-Hernández S, Alquicira-Hernández K, López-Fuentes A, Porrón-Sotelo L, Huerta AM, Bonavides-Martínez C, Balderas-Martínez YI, Pannier L, Olvera M, Labastida A, Jiménez-Jacinto V, Vega-Alvarado L, Del Moral-Chávez V, Hernández-Alvarez A, Morett E, Collado-Vides J., 2012, RegulonDB v8.0: omics data sets, evolutionary conservation, regulatory phrases, cross-validated gold standards and more., Nucleic Acids Res.

 [11] Zaslaver A., Bren A., Ronen M., Itzkovitz S., Kikoin I., Shavit S., Liebermeister W., Surette MG., Alon U., 2006, A comprehensive library of fluorescent transcriptional reporters for Escherichia coli., Nat Methods 3(8):623-8

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