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Escherichia coli K-12 substr. MG1655 RNA: tmRNA



Gene: ssrA Accession Numbers: EG30100 (EcoCyc), b2621, ECK2617

Synonyms: sipB, 10Sa RNA, transfer-messenger RNA

Superclasses: tmRNA

Regulation Summary Diagram: ?

Summary:
SsrA RNA functions to release a stalled ribosome from the end of a "broken" mRNA that has no stop codon by acting both as a tRNA and as an mRNA, using a "trans-translation" mechanism [Muto96]. SsrA also mediates release of a ribosome that has stalled due to lack of an appropriate tRNA [Roche99, Hayes02]. Other translation problems can also lead to SsrA activity [Ueda02, Abo02, Hayes02a, Sunohara02, Christensen03]. In addition, SsrA RNA stimulates degradation of defective mRNAs [Yamamoto03a].

The SsrA RNA contains a tRNA-like structural region that is processed by RNase P and charged by alanyl-tRNA synthetase [Komine94, Himeno97]. The SsrA RNA also has a region that acts as a messenger RNA and encodes a translated tag [Tu95, Himeno97] that is added to the nascent protein and which targets this protein for degradation [Keiler96, Gottesman98, Herman98, Smith99a, Kim00b, Singh00, Levchenko00, Reid01, Lo01, Burton01, Flynn01, Navon01, Spiers02, Flynn03, Burton03]. SsrA-tagged proteins are degraded with zero-order kinetics at the single-cell level [Wong07].

The structure of the SsrA RNA [Felden96, Felden97, Nameki99, Nameki99a, HanawaSuetsugu01, Gaudin03, Gutmann03] and the translational mechanism [Williams99, Bordeau02] have been examined in detail. SsrA RNA interacts with tRNA(Ala) [Gillet01], with elongation factor Tu [Zvereva01, Barends01], and with ribosomal protein S1 [Bordeau02]. SsrA also binds to SspB, which is a factor that confers specificity on the activity of ClpXP protease [Wah02]. A crystal structure of SspB bound to an SsrA-encoded tag peptide is presented [Song03]. Under some circumstances, SsrA may compete with the activity of the translational release factor RF2 [Collier02]. Alanine-aminoacylated [Tadaki96] SsrA binds specifically to 70S ribosomes [Komine96, Tadaki96]. SsrA ribosome association and its activity require the SmpB protein [Karzai99], which binds to SsrA RNA [Karzai99, Barends01]. SsrA and SmpB are found in a larger complex also containing ribosomal protein S1, phosphoribosyl pyrophosphate synthase, RNase R, and YfbG [Karzai01]. SmpB and elongation factor Tu exhibit chaperone activity toward SsrA RNA [Corvaisier03]. A crystal structure of SsrA RNA bound to SmpB is presented at 3.2 A resolution [Gutmann03].

The tRNA functionality is required for the mRNA functionality of SsrA [Himeno97a]. The aminoglycoside antibiotic neomycin B interferes with aminoacylation of SsrA [Corvaisier03]. RelE, which downregulates translation in response to starvation, cleaves SsrA RNA as well as mRNA, and SsrA is involved in recovery from a RelE stress response [Christensen03].

The lacI mRNA appears to be a physiologically-relevant SsrA system substrate [Abo00, Roche01]; other substrates detected in vivo include mRNAs encoding lambda cI repressor, YbeL, GalE, RbsK, and a SlyD-kan(R) fusion protein [Roche01], mRNAs subject to amber or ochre tRNA suppression [Ueda02], and mRNAs whose translation is affected by miscoding antibiotic drugs [Abo02].

The SsrA RNA is transcribed as a larger precursor RNA that is processed to form the mature RNA [Subbarao89, Chauhan89, Srivastava90, Srivastava92, Makarov92, Komine94, Li98, LinChao99].

An ssrA mutant exhibits a growth defect [Oh91, Komine94] and a motility defect [Komine94]. An ssrA mutation causes increased RelE-mediated toxicity and ssrA overexpression causes decreased toxicity, compared to wild type [Christensen03]. A sipB391 mutation causes a defect in growth of lambda immP22, which is a hybrid bacteriophage [Strauch86]. An ssrA mutation causes a defect in regulation of Mu lysogeny [Ranquet01], and SsrA may exert regulatory effects via tagging of repressor molecules [OHandley02]. SsrA affects DNA binding by the phage proteins [Retallack94, Retallack95] and has been observed to bind directly to these proteins [Retallack95], although this interaction is nonspecific and appears not to be responsible for the phage growth phenotype [Withey99]. The SsrA RNA and the Prs phosphoribosyl pyrophosphate synthetase exhibit a genetic interaction [Ando96]. An ssrA deletion mutant is sensitive to cell envelope stress [Hobbs10].

The tmRNA genes have been used as probes for identification of bacterial species [Schonhuber01, Schonhuber01a].

Reviews: [Janosi96, Muto96, Muto98, Wassarman99, Karzai00, Jentsch96, Zvereva00, Wower01, Gillet01a, Withey02, Withey03].

Citations: [Oh90, Kirby94, Nakano01, Williams03]

Map Position: [2,753,615 -> 2,753,977] (59.35 centisomes)
Length: 363 bp

Reactions known to produce the compound:

tRNA processing :
a tRNA precursor with a 5' extension and a short 3' extension + H2O → a tRNA precursor with a short 3' extension + a single-stranded RNA
a tRNA precursor with a 5' extension + H2O → an uncharged tRNA + a single-stranded RNA

Not in pathways:
an mRNA + H2O → a single-stranded RNA + a single-stranded RNA
an mRNA + H2O → a single-stranded RNA + a single-stranded RNA
RNase E degradation substrate mRNA + n H2O → n a single-stranded RNA
YhaV endonuclease degradation substrate rRNA + H2O → 2 a single-stranded RNA
YhaV endonuclease degradation substrate mRNA + H2O → 2 a single-stranded RNA
RNase III mRNA processing substrate + 2 H2O → RNase III processing product mRNA + 2 a single-stranded RNA
23S rRNA[periplasmic space] + H2O[periplasmic space] → 2 a single-stranded RNA[periplasmic space]
an mRNA[periplasmic space] + H2O[periplasmic space] → 2 a single-stranded RNA[periplasmic space]
RNase G degradation substrate mRNA + H2O → 2 a single-stranded RNA
9S rRNA + 2 H2O → 5S rRNA + 2 a single-stranded RNA
RNase E mRNA processing substrate + n H2O → RNase E processing product mRNA + n a single-stranded RNA

Reactions known to both consume and produce the compound:

Not in pathways:
a single-stranded RNA + phosphate ↔ a single-stranded RNA + a nucleoside diphosphate

In Reactions of unknown directionality:

Not in pathways:
rRNA[periplasmic space] = 2 a single-stranded RNA[periplasmic space]

Unification Links: ASAP:ABE-0008624 , CGSC:35783 , EchoBASE:EB4263 , EcoGene:EG30100 , EcoliWiki:b2621 , OU-Microarray:b2621 , PortEco:ssrA , RegulonDB:EG30100

GO Terms:

Biological Process: GO:0070929 - trans-translation Inferred from experiment [Keiler96]
GO:0070930 - trans-translation-dependent protein tagging Inferred from experiment [Keiler96]
GO:0072344 - rescue of stalled ribosome Inferred from experiment [Keiler96, Muto96]
Cellular Component: GO:0005737 - cytoplasm
GO:0005829 - cytosol

MultiFun Terms: cell processes protection drug resistance/sensitivity
cell structure ribosomes
information transfer protein related translation
information transfer protein related turnover, degradation
information transfer RNA related RNA degradation
regulation type of regulation posttranscriptional


Gene Local Context (not to scale): ?

Transcription Unit:

Notes:

History:
Suzanne Paley on Thu Oct 21, 2004:
Position updated based on U00096.2 release of genome
7/10/1998 (pkarp) Merged genes G325/sipB and EG30100/ssrA
10/20/97 Gene b2621 from Blattner lab Genbank (v. M52) entry merged into EcoCyc gene EG30100.


References

Abo00: Abo T, Inada T, Ogawa K, Aiba H (2000). "SsrA-mediated tagging and proteolysis of LacI and its role in the regulation of lac operon." EMBO J 19(14);3762-9. PMID: 10899129

Abo02: Abo T, Ueda K, Sunohara T, Ogawa K, Aiba H (2002). "SsrA-mediated protein tagging in the presence of miscoding drugs and its physiological role in Escherichia coli." Genes Cells 7(7);629-38. PMID: 12081641

Ando96: Ando H, Kitabatake M, Inokuchi H (1996). "10Sa RNA complements the temperature-sensitive phenotype caused by a mutation in the phosphoribosyl pyrophosphate synthetase (prs) gene in Escherichia coli." Genes Genet Syst 71(1);47-50. PMID: 8925474

Barends01: Barends S, Karzai AW, Sauer RT, Wower J, Kraal B (2001). "Simultaneous and functional binding of SmpB and EF-Tu-TP to the alanyl acceptor arm of tmRNA." J Mol Biol 314(1);9-21. PMID: 11724528

Bordeau02: Bordeau V, Felden B (2002). "Ribosomal protein S1 induces a conformational change of tmRNA; more than one protein S1 per molecule of tmRNA." Biochimie 84(8);723-9. PMID: 12457560

Burton01: Burton RE, Siddiqui SM, Kim YI, Baker TA, Sauer RT (2001). "Effects of protein stability and structure on substrate processing by the ClpXP unfolding and degradation machine." EMBO J 20(12);3092-100. PMID: 11406586

Burton03: Burton RE, Baker TA, Sauer RT (2003). "Energy-dependent degradation: Linkage between ClpX-catalyzed nucleotide hydrolysis and protein-substrate processing." Protein Sci 12(5);893-902. PMID: 12717012

Chauhan89: Chauhan AK, Apirion D (1989). "The gene for a small stable RNA (10Sa RNA) of Escherichia coli." Mol Microbiol 3(11);1481-5. PMID: 2482406

Christensen03: Christensen SK, Gerdes K (2003). "RelE toxins from bacteria and Archaea cleave mRNAs on translating ribosomes, which are rescued by tmRNA." Mol Microbiol 48(5);1389-400. PMID: 12787364

Collier02: Collier J, Binet E, Bouloc P (2002). "Competition between SsrA tagging and translational termination at weak stop codons in Escherichia coli." Mol Microbiol 45(3);745-54. PMID: 12139620

Corvaisier03: Corvaisier S, Bordeau V, Felden B (2003). "Inhibition of transfer messenger RNA aminoacylation and trans-translation by aminoglycoside antibiotics." J Biol Chem 278(17);14788-97. PMID: 12588865

Felden96: Felden B, Himeno H, Muto A, Atkins JF, Gesteland RF (1996). "Structural organization of Escherichia coli tmRNA." Biochimie 78(11-12);979-83. PMID: 9150875

Felden97: Felden B, Himeno H, Muto A, McCutcheon JP, Atkins JF, Gesteland RF (1997). "Probing the structure of the Escherichia coli 10Sa RNA (tmRNA)." RNA 3(1);89-103. PMID: 8990402

Flynn01: Flynn JM, Levchenko I, Seidel M, Wickner SH, Sauer RT, Baker TA (2001). "Overlapping recognition determinants within the ssrA degradation tag allow modulation of proteolysis." Proc Natl Acad Sci U S A 98(19);10584-9. PMID: 11535833

Flynn03: Flynn JM, Neher SB, Kim YI, Sauer RT, Baker TA (2003). "Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals." Mol Cell 11(3);671-83. PMID: 12667450

Gaudin03: Gaudin C, Nonin-Lecomte S, Tisne C, Corvaisier S, Bordeau V, Dardel F, Felden B (2003). "The tRNA-like domains of E coli and A.aeolicus transfer-messenger RNA: structural and functional studies." J Mol Biol 331(2);457-71. PMID: 12888352

Gillet01: Gillet R, Felden B (2001). "Transfer RNA(Ala) recognizes transfer-messenger RNA with specificity; a functional complex prior to entering the ribosome?." EMBO J 20(11);2966-76. PMID: 11387229

Gillet01a: Gillet R, Felden B (2001). "Emerging views on tmRNA-mediated protein tagging and ribosome rescue." Mol Microbiol 42(4);879-85. PMID: 11737633

Gottesman98: Gottesman S, Roche E, Zhou Y, Sauer RT (1998). "The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system." Genes Dev 12(9);1338-47. PMID: 9573050

Gutmann03: Gutmann S, Haebel PW, Metzinger L, Sutter M, Felden B, Ban N (2003). "Crystal structure of the transfer-RNA domain of transfer-messenger RNA in complex with SmpB." Nature 424(6949);699-703. PMID: 12904796

HanawaSuetsugu01: Hanawa-Suetsugu K, Bordeau V, Himeno H, Muto A, Felden B (2001). "Importance of the conserved nucleotides around the tRNA-like structure of Escherichia coli transfer-messenger RNA for protein tagging." Nucleic Acids Res 29(22);4663-73. PMID: 11713316

Hayes02: Hayes CS, Bose B, Sauer RT (2002). "Stop codons preceded by rare arginine codons are efficient determinants of SsrA tagging in Escherichia coli." Proc Natl Acad Sci U S A 99(6);3440-5. PMID: 11891313

Hayes02a: Hayes CS, Bose B, Sauer RT (2002). "Proline residues at the C terminus of nascent chains induce SsrA tagging during translation termination." J Biol Chem 277(37);33825-32. PMID: 12105207

Herman98: Herman C, Thevenet D, Bouloc P, Walker GC, D'Ari R (1998). "Degradation of carboxy-terminal-tagged cytoplasmic proteins by the Escherichia coli protease HflB (FtsH)." Genes Dev 12(9);1348-55. PMID: 9573051

Himeno97: Himeno H, Sato M, Tadaki T, Fukushima M, Ushida C, Muto A (1997). "In vitro trans translation mediated by alanine-charged 10Sa RNA." J Mol Biol 268(5);803-8. PMID: 9180372

Himeno97a: Himeno H, Nameki N, Tadaki T, Sato M, Hanawa K, Fukushima M, Ishii M, Ushida C, Muto A (1997). "Escherichia coli tmRNA (10Sa RNA) in trans-translation." Nucleic Acids Symp Ser (37);185-6. PMID: 9586061

Hobbs10: Hobbs EC, Astarita JL, Storz G (2010). "Small RNAs and Small Proteins Involved in Resistance to Cell Envelope Stress and Acid Shock in Escherichia coli: Analysis of a Bar-coded Mutant Collection." J Bacteriol 192(1):59-62. PMID: 19734312

Janosi96: Janosi L, Ricker R, Kaji A (1996). "Dual functions of ribosome recycling factor in protein biosynthesis: disassembling the termination complex and preventing translational errors." Biochimie 78(11-12);959-69. PMID: 9150873

Jentsch96: Jentsch S (1996). "When proteins receive deadly messages at birth." Science 271(5251);955-6. PMID: 8584931

Karzai00: Karzai AW, Roche ED, Sauer RT (2000). "The SsrA-SmpB system for protein tagging, directed degradation and ribosome rescue." Nat Struct Biol 7(6);449-55. PMID: 10881189

Karzai01: Karzai AW, Sauer RT (2001). "Protein factors associated with the SsrA.SmpB tagging and ribosome rescue complex." Proc Natl Acad Sci U S A 98(6);3040-4. PMID: 11248028

Karzai99: Karzai AW, Susskind MM, Sauer RT (1999). "SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA)." EMBO J 18(13);3793-9. PMID: 10393194

Keiler96: Keiler KC, Waller PR, Sauer RT (1996). "Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA." Science 271(5251);990-3. PMID: 8584937

Kim00b: Kim YI, Burton RE, Burton BM, Sauer RT, Baker TA (2000). "Dynamics of substrate denaturation and translocation by the ClpXP degradation machine." Mol Cell 5(4);639-48. PMID: 10882100

Kirby94: Kirby JE, Trempy JE, Gottesman S (1994). "Excision of a P4-like cryptic prophage leads to Alp protease expression in Escherichia coli." J Bacteriol 176(7);2068-81. PMID: 7511583

Komine94: Komine Y, Kitabatake M, Yokogawa T, Nishikawa K, Inokuchi H (1994). "A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli." Proc Natl Acad Sci U S A 91(20);9223-7. PMID: 7524073

Komine96: Komine Y, Kitabatake M, Inokuchi H (1996). "10Sa RNA is associated with 70S ribosome particles in Escherichia coli." J Biochem (Tokyo) 119(3);463-7. PMID: 8830040

Levchenko00: Levchenko I, Seidel M, Sauer RT, Baker TA (2000). "A specificity-enhancing factor for the ClpXP degradation machine." Science 289(5488);2354-6. PMID: 11009422

Li98: Li Z, Pandit S, Deutscher MP (1998). "3' exoribonucleolytic trimming is a common feature of the maturation of small, stable RNAs in Escherichia coli." Proc Natl Acad Sci U S A 95(6);2856-61. PMID: 9501180

LinChao99: Lin-Chao S, Wei CL, Lin YT (1999). "RNase E is required for the maturation of ssrA RNA and normal ssrA RNA peptide-tagging activity." Proc Natl Acad Sci U S A 96(22);12406-11. PMID: 10535935

Lo01: Lo JH, Baker TA, Sauer RT (2001). "Characterization of the N-terminal repeat domain of Escherichia coli ClpA-A class I Clp/HSP100 ATPase." Protein Sci 10(3);551-9. PMID: 11344323

Makarov92: Makarov EM, Apirion D (1992). "10Sa RNA: processing by and inhibition of RNase III." Biochem Int 26(6);1115-24. PMID: 1378735

Muto96: Muto A, Sato M, Tadaki T, Fukushima M, Ushida C, Himeno H (1996). "Structure and function of 10Sa RNA: trans-translation system." Biochimie 78(11-12);985-91. PMID: 9150876

Muto98: Muto A, Ushida C, Himeno H (1998). "A bacterial RNA that functions as both a tRNA and an mRNA." Trends Biochem Sci 23(1);25-9. PMID: 9478132

Nakano01: Nakano H, Goto S, Nakayashiki T, Inokuchi H (2001). "Temperature-sensitive mutations in various genes of Escherichia coli K12 can be suppressed by the ssrA gene for 10Sa RNA (tmRNA)." Mol Genet Genomics 265(4);615-21. PMID: 11459181

Nameki99: Nameki N, Felden B, Atkins JF, Gesteland RF, Himeno H, Muto A (1999). "Functional and structural analysis of a pseudoknot upstream of the tag-encoded sequence in E. coli tmRNA." J Mol Biol 286(3);733-44. PMID: 10024447

Nameki99a: Nameki N, Chattopadhyay P, Himeno H, Muto A, Kawai G (1999). "An NMR and mutational analysis of an RNA pseudoknot of Escherichia coli tmRNA involved in trans-translation." Nucleic Acids Res 27(18);3667-75. PMID: 10471735

Navon01: Navon A, Goldberg AL (2001). "Proteins are unfolded on the surface of the ATPase ring before transport into the proteasome." Mol Cell 8(6);1339-49. PMID: 11779508

Oh90: Oh BK, Chauhan AK, Isono K, Apirion D (1990). "Location of a gene (ssrA) for a small, stable RNA (10Sa RNA) in the Escherichia coli chromosome." J Bacteriol 172(8);4708-9. PMID: 1695897

Oh91: Oh BK, Apirion D (1991). "10Sa RNA, a small stable RNA of Escherichia coli, is functional." Mol Gen Genet 229(1);52-6. PMID: 1716727

OHandley02: O'Handley D, Nakai H (2002). "Derepression of bacteriophage mu transposition functions by truncated forms of the immunity repressor." J Mol Biol 322(2);311-24. PMID: 12217693

Ranquet01: Ranquet C, Geiselmann J, Toussaint A (2001). "The tRNA function of SsrA contributes to controlling repression of bacteriophage Mu prophage." Proc Natl Acad Sci U S A 98(18);10220-5. PMID: 11517307

Reid01: Reid BG, Fenton WA, Horwich AL, Weber-Ban EU (2001). "ClpA mediates directional translocation of substrate proteins into the ClpP protease." Proc Natl Acad Sci U S A 98(7);3768-72. PMID: 11259663

Retallack94: Retallack DM, Johnson LL, Friedman DI (1994). "Role for 10Sa RNA in the growth of lambda-P22 hybrid phage." J Bacteriol 176(7);2082-9. PMID: 8144474

Retallack95: Retallack DM, Friedman DI (1995). "A role for a small stable RNA in modulating the activity of DNA-binding proteins." Cell 83(2);227-35. PMID: 7585940

Roche01: Roche ED, Sauer RT (2001). "Identification of endogenous SsrA-tagged proteins reveals tagging at positions corresponding to stop codons." J Biol Chem 276(30);28509-15. PMID: 11373298

Roche99: Roche ED, Sauer RT (1999). "SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity." EMBO J 18(16);4579-89. PMID: 10449423

Schonhuber01: Schonhuber W, Le Bourhis G, Tremblay J, Amann R, Kulakauskas S (2001). "Utilization of tmRNA sequences for bacterial identification." BMC Microbiol 1(1);20. PMID: 11560762

Schonhuber01a: Schonhuber W, Le Bourhis G, Tremblay J, Amann R, Kulakauskas S (2001). "Utilization of tmRNA sequences for bacterial identification." BMC Microbiol 1(1);20. PMID: 12365411

Singh00: Singh SK, Grimaud R, Hoskins JR, Wickner S, Maurizi MR (2000). "Unfolding and internalization of proteins by the ATP-dependent proteases ClpXP and ClpAP." Proc Natl Acad Sci U S A 97(16);8898-903. PMID: 10922052

Smith99a: Smith CK, Baker TA, Sauer RT (1999). "Lon and Clp family proteases and chaperones share homologous substrate-recognition domains." Proc Natl Acad Sci U S A 96(12);6678-82. PMID: 10359771

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Williams99: Williams KP, Martindale KA, Bartel DP (1999). "Resuming translation on tmRNA: a unique mode of determining a reading frame." EMBO J 18(19);5423-33. PMID: 10508174

Withey02: Withey JH, Friedman DI (2002). "The biological roles of trans-translation." Curr Opin Microbiol 5(2);154-9. PMID: 11934611

Withey03: Withey JH, Friedman DI (2003). "A Salvage Pathway for Protein Synthesis: tmRNA and Trans-Translation." Annu Rev Microbiol 57:101-23. PMID: 12730326

Withey99: Withey J, Friedman D (1999). "Analysis of the role of trans-translation in the requirement of tmRNA for lambdaimmP22 growth in Escherichia coli." J Bacteriol 181(7);2148-57. PMID: 10094693

Wong07: Wong WW, Tsai TY, Liao JC (2007). "Single-cell zeroth-order protein degradation enhances the robustness of synthetic oscillator." Mol Syst Biol 3;130. PMID: 17667952

Wower01: Wower J, Wower IK, Kraal B, Zwieb CW (2001). "Quality control of the elongation step of protein synthesis by tmRNP." J Nutr 131(11);2978S-82S. PMID: 11694632

Yamamoto03a: Yamamoto Y, Sunohara T, Jojima K, Inada T, Aiba H (2003). "SsrA-mediated trans-translation plays a role in mRNA quality control by facilitating degradation of truncated mRNAs." RNA 9(4);408-18. PMID: 12649493

Zvereva00: Zvereva ME, Shpanchenko OV, Dontsova OA, Bogdanov AA (2000). "[Structure and function of tmRNA (10Sa RNK)]." Mol Biol (Mosk) 34(6);1081-9. PMID: 11186008

Zvereva01: Zvereva MI, Ivanov PV, Teraoka Y, Topilina NI, Dontsova OA, Bogdanov AA, Kalkum M, Nierhaus KH, Shpanchenko OV (2001). "Complex of transfer-messenger RNA and elongation factor Tu. Unexpected modes of interaction." J Biol Chem 276(50);47702-8. PMID: 11595738

Other References Related to Gene Regulation

Vvedenskaya12: Vvedenskaya IO, Sharp JS, Goldman SR, Kanabar PN, Livny J, Dove SL, Nickels BE (2012). "Growth phase-dependent control of transcription start site selection and gene expression by nanoRNAs." Genes Dev 26(13);1498-507. PMID: 22751503


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Please cite the following article in publications resulting from the use of EcoCyc: Nucleic Acids Research 41:D605-12 2013
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