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Escherichia coli K-12 substr. MG1655 Transporter: nitrate reductase A

Synonyms: NRA

Subunit composition of nitrate reductase A = [NarG]2[NarH]2[NarI]2
         nitrate reductase A, α subunit = NarG (summary available)
         nitrate reductase A, β subunit = NarH (summary available)
         nitrate reductase A, γ subunit = NarI (extended summary available)

Summary:
narGHI encodes a membrane bound quinol-nitrate oxidoreductase, known as nitrate reductase A (NRA) in E. coli K-12. Nitrate reductase A is a respiratory enzyme that functions as a terminal reductase in electron transport pathways that operate during anaerobic growth in the presence of nitrate (see reviews by [Berks95] and [Unden97]).

The NRA heterotrimer consists of a molybdenum cofactor containing α subunit (NarG), an Fe-S cluster containing β subunit (NarH) and a heme containing γ subunit (NarI) [MacGregor74, Forget74, Clegg76, Enoch75, Sodergren88]. The redox active prosthetic groups of NRA form an electron transport chain which uses electrons from the membrane quinone pool for the reduction of cytoplasmic nitrate [Bertero03]. Electrons derived from the oxidation of quinol are transferred through two hemes in NarI, one [3Fe-4S] (known as FS4) and three [4Fe-4S] clusters (FS3, FS2 and FS1) in NarH and one [4Fe-4S] (FS0) cluster in NarG to the Mos-bisPGD cofactor where nitrate is reduced to nitrite [Rothery99, Zhao03, Rothery01, Rothery04]

Nitrate reductase A can use both ubiquinol and menaquinol as electron donors [Wissenbach90, Wissenbach92]. Nitrate reductase A has a H+/e- ratio of 1 [Unden97].

A crystal structure of the catalytic and electron transfer subunits (NarG and NarH) has been solved at 2.0 Å resolution [Jormakka04], and structures of the NarGHI complex both alone and in complex with the quinol binding site (Q-site) inhibitor pentachlorophenol have been solved at 1.9 and 2 Å resolution [Bertero03, Bertero05]. NarGH is localised on the cytosolic side of the inner membrane and interacts with the membrane bound NarI subunit through a hydrophobic interface. Eight redox centres form an arc through the centre of the heterotrimer and are suggestive of a pathway for electron transfer from menaquinol to the nitrate reducing site in NarG. NarGHI forms a homodimer in vitro and probably in vivo [Bertero03].

A fourth polypeptide encoded by the narJ gene, is required for the incorporation of the molybdenum cofactor into NarG, the α subunit [Dubourdieu92, Blasco92, Blasco98]. If it is coexpressed with the private chaperone NarJ, the NarGH complex alone is soluble and active with artificial electron donors such as benzyl viologen. NarGH becomes localized to the cytoplasmic side of the inner membrane by interaction with NarI [Blasco92].

Nitrate reductase is responsible for the tellurite reductase activity associated with E. coli membranes. An E. coli strain lacking the membrane associated nitrate reductases is hypersensitive to tellurite under aerobic conditions. A mutant strain which synthesizes nitrate reductase A in large quantities can grow anaereobically with tellurite as the sole electron acceptor. It is not clear whether nitrate reductase is responsible for the total reduction of tellurite to elemental tellurium or whether this reaction is the result of two steps [Avazeri97].

narGHJ and I form an operon in E. coli K-12 which is induced upon anaerobic growth in the presence of nitrate [Sodergren88a]. narGHJI is weakly expressed when nitrate levels are low and maximally expressed when nitrate levels are high [Wang99a]

E. coli K-12 contains three nitrate reductases. Two of them, nitrate reductase A (NRA) and nitrate reductase Z (NRZ), are membrane bound and biochemically similar (reviewed in [Bonnefoy94]. The third nitrate reductase, Nap, is located in the periplasm [Grove96].

nar: nitrate reductase [Stewart82]

Reviews: [Blasco01]

Citations: [Fedor14, Garland75, Kristjansson79, Jones80, Morpeth85, vanderOost96, MacGregor75, MacGregor76, Magalon97, Rothery01a, Rothery98, Magalon98, Grimaldi10, Zhao03a, Grimaldi12, Grimaldi05, Lanciano07, AriasCartin10, Fedor14a, Jones11, Zakian10, Rothery10, Giordani04, Magalon98a, Magalon97a, Tseng94, Rabin92, Guigliarelli92, Vincent78, Vincent79, Blum82]

Locations: inner membrane

Relationship Links: PDB:Structure:1Q16 , PDB:Structure:1SIW , PDB:Structure:1Y4Z , PDB:Structure:1Y5I , PDB:Structure:1Y5L , PDB:Structure:1Y5N

Gene-Reaction Schematic: ?

GO Terms:

Biological Process: GO:0009061 - anaerobic respiration Inferred from experiment [Li87, Showe68]
GO:0006810 - transport Inferred by computational analysis [GOA00]
Molecular Function: GO:0008940 - nitrate reductase activity Inferred by computational analysis Inferred from experiment [Stewart82, Forget74, Rondeau84, GOA01a, GOA01]
GO:0009055 - electron carrier activity Inferred from experiment [Jones80, RuizHerrera69]
GO:0048038 - quinone binding Inferred from experiment [Brito95]
Cellular Component: GO:0005886 - plasma membrane Inferred from experiment [Clegg76]
GO:0009325 - nitrate reductase complex Inferred by computational analysis Inferred from experiment [Forget74, GOA01]
GO:0031224 - intrinsic component of membrane Inferred from experiment [Garland75]
GO:0031235 - intrinsic component of the cytoplasmic side of the plasma membrane Inferred from experiment [Bertero03]
GO:0044799 - NarGHI complex Inferred from experiment [Bertero03, Forget74]

Credits:
Curated 28-Apr-2008 by Nolan L , Macquarie University
Revised 29-Jul-2014 by Mackie A , Macquarie University
Last-Curated ? 30-Jul-2014 by Mackie A , Macquarie University


Enzymatic reaction of: nitrate reductase

Synonyms: respiratory nitrate reductase, nitrite:(acceptor) oxidoreductase

EC Number: 1.7.5.1

Alternative Substrates for nitrate: chlorate [Forget74 ]

In Pathways: nitrate reduction III (dissimilatory) , nitrate reduction VIII (dissimilatory)

Cofactors or Prosthetic Groups: a [4Fe-4S] iron-sulfur cluster [Comment 1], [3Fe-4S] iron-sulfur cluster , guanylyl molybdenum cofactor

Inhibitors (Competitive): azide [Forget74]

Inhibitors (Unknown Mechanism): 2-n-heptyl-4-hydroxyquinoline-N-oxide [Rothery99] , stigmatellin [Rothery99] , hydrogen cyanide [Forget74]


Enzymatic reaction of: tellurite reductase (nitrate reductase A)

EC Number: 1.97.1.-

tellurite + a reduced electron acceptor <=> Te0 + an oxidized electron acceptor

The reaction direction shown, that is, A + B ↔ C + D versus C + D ↔ A + B, is in accordance with the direction in which it was curated.

The reaction is favored in the direction shown.

Summary:
Tellurite reductase activity was measured using benzyl viologen as an electron donor [Avazeri97]


Subunit of nitrate reductase A: nitrate reductase A, α subunit

Synonyms: ChlC, NarC, NarG

Gene: narG Accession Numbers: EG10638 (EcoCyc), b1224, ECK1218

Locations: inner membrane

Sequence Length: 1247 AAs

Molecular Weight: 140.49 kD (from nucleotide sequence)

pI: 6.49

GO Terms:

Biological Process: GO:0009061 - anaerobic respiration Inferred from experiment [Sodergren88a]
GO:0042126 - nitrate metabolic process Inferred from experiment Inferred by computational analysis [GOA01, Stewart82]
GO:0042128 - nitrate assimilation Inferred by computational analysis [UniProtGOA11]
GO:0055114 - oxidation-reduction process Inferred by computational analysis [UniProtGOA11, GOA01]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [Rajagopala14, Chan10, Chan09a, Lasserre06, Vergnes06, Banci05, Bertero03, Zakian10, Rothery04, Butland05]
GO:0008940 - nitrate reductase activity Inferred from experiment Inferred by computational analysis [GOA01a, GOA01, Stewart82, Rondeau84, Forget74]
GO:0009055 - electron carrier activity Inferred from experiment Inferred by computational analysis [GOA01, Bertero03, Rothery04]
GO:0043546 - molybdopterin cofactor binding Inferred from experiment [Bertero03]
GO:0051539 - 4 iron, 4 sulfur cluster binding Inferred from experiment Inferred by computational analysis [UniProtGOA11, GOA01, Bertero03]
GO:0016491 - oxidoreductase activity Inferred by computational analysis [UniProtGOA11, GOA01]
GO:0016651 - oxidoreductase activity, acting on NAD(P)H Inferred by computational analysis [Gaudet10]
GO:0030151 - molybdenum ion binding Inferred by computational analysis [GOA01]
GO:0046872 - metal ion binding Inferred by computational analysis [UniProtGOA11]
GO:0051536 - iron-sulfur cluster binding Inferred by computational analysis [UniProtGOA11]
Cellular Component: GO:0016020 - membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11, Lasserre06]
GO:0031224 - intrinsic component of membrane Inferred from experiment [Garland75]
GO:0031235 - intrinsic component of the cytoplasmic side of the plasma membrane Inferred from experiment [Bertero03]
GO:0044799 - NarGHI complex Inferred from experiment [Bertero03, Forget74]
GO:0005886 - plasma membrane Inferred by computational analysis [UniProtGOA11a, UniProtGOA11]
GO:0009325 - nitrate reductase complex Inferred by computational analysis [GOA01]

MultiFun Terms: metabolism energy metabolism, carbon anaerobic respiration
metabolism energy production/transport electron acceptors

Isozyme Sequence Similarity:
nitrate reductase Z, α subunit: YES

Unification Links: DIP:DIP-10311N , EcoliWiki:b1224 , Mint:MINT-1233973 , ModBase:P09152 , PR:PRO_000023351 , Pride:P09152 , Protein Model Portal:P09152 , RefSeq:NP_415742 , SMR:P09152 , String:511145.b1224 , UniProt:P09152

Relationship Links: InterPro:IN-FAMILY:IPR006468 , InterPro:IN-FAMILY:IPR006655 , InterPro:IN-FAMILY:IPR006656 , InterPro:IN-FAMILY:IPR006657 , InterPro:IN-FAMILY:IPR006963 , InterPro:IN-FAMILY:IPR009010 , InterPro:IN-FAMILY:IPR027467 , InterPro:IN-FAMILY:IPR028189 , PDB:Structure:1Q16 , PDB:Structure:1R27 , PDB:Structure:1SIW , PDB:Structure:1Y4Z , PDB:Structure:1Y5I , PDB:Structure:1Y5L , PDB:Structure:1Y5N , PDB:Structure:3EGW , PDB:Structure:3IR5 , PDB:Structure:3IR6 , PDB:Structure:3IR7 , Pfam:IN-FAMILY:PF00384 , Pfam:IN-FAMILY:PF01568 , Pfam:IN-FAMILY:PF14710 , Prosite:IN-FAMILY:PS00490 , Prosite:IN-FAMILY:PS00551 , Prosite:IN-FAMILY:PS00932 , Prosite:IN-FAMILY:PS51669 , Smart:IN-FAMILY:SM00926

Summary:
The α subunit of nitrate reductase A contains the molybdenum cofactor - molybdo-bis(molybdopterin guanine dinucleotide) or Mo-bisMGD and is the site of nitrate reduction. In addition, an [4Fe-4S] cluster (FS0) with unusual coordination - 1 histidine (H50) and 3 cysteine residues (C54, C58, C93) - and a high-spin ground state was detected in the crystal structure [Bertero03, Jormakka04, Rothery04]. NarG contains 4 conserved α-β domains grouped around the cofactor [Bertero03]. The assembly of FS0 in nitrate reductase A is a prerequisite for Mo-bisMGD insertion [Rothery10].

The NarJ chaperone interacts specifically with NarG [Blasco98]. The N-terminal region of NarG interacts with NarJ [Vergnes06, Chan06, Li09b, Zakian10]. NarG contains a vestige leader sequence [Turner04]

nar: nitrate reductase; chl: chlorate resistant [Stewart82]

Essentiality data for narG knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 2]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 3]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 4]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 3]
Yes [Feist07, Comment 5]

Subunit of nitrate reductase A: nitrate reductase A, β subunit

Synonyms: ChlC, NarH

Gene: narH Accession Numbers: EG10639 (EcoCyc), b1225, ECK1219

Locations: inner membrane

Sequence Length: 512 AAs

Molecular Weight: 58.066 kD (from nucleotide sequence)

pI: 5.68

GO Terms:

Biological Process: GO:0009061 - anaerobic respiration Inferred from experiment [Sodergren88a]
GO:0042126 - nitrate metabolic process Inferred from experiment Inferred by computational analysis [GOA01, Stewart82]
GO:0042128 - nitrate assimilation Inferred by computational analysis [UniProtGOA11]
GO:0055114 - oxidation-reduction process Inferred by computational analysis [UniProtGOA11, GOA01]
Molecular Function: GO:0005515 - protein binding Inferred from experiment [Rajagopala14, Lasserre06, Vergnes06, Banci05, Bertero03, Rothery04, Butland05]
GO:0008940 - nitrate reductase activity Inferred from experiment Inferred by computational analysis [GOA01a, GOA01, Stewart82]
GO:0009055 - electron carrier activity Inferred from experiment [Guigliarelli92]
GO:0051538 - 3 iron, 4 sulfur cluster binding Inferred from experiment Inferred by computational analysis [UniProtGOA11, Johnson85]
GO:0051539 - 4 iron, 4 sulfur cluster binding Inferred from experiment Inferred by computational analysis [UniProtGOA11, Johnson85]
GO:0016491 - oxidoreductase activity Inferred by computational analysis [UniProtGOA11]
GO:0046872 - metal ion binding Inferred by computational analysis [UniProtGOA11]
GO:0051536 - iron-sulfur cluster binding Inferred by computational analysis [UniProtGOA11, GOA01, Blasco89]
Cellular Component: GO:0016020 - membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11, Lasserre06]
GO:0031224 - intrinsic component of membrane Inferred from experiment [Garland75]
GO:0031235 - intrinsic component of the cytoplasmic side of the plasma membrane Inferred from experiment [Bertero03]
GO:0044799 - NarGHI complex Inferred from experiment [Bertero03, Forget74]
GO:0005886 - plasma membrane Inferred by computational analysis [UniProtGOA11a, UniProtGOA11]
GO:0009325 - nitrate reductase complex Inferred by computational analysis [GOA01]

MultiFun Terms: metabolism energy metabolism, carbon anaerobic respiration
metabolism energy production/transport electron acceptors

Isozyme Sequence Similarity:
nitrate reductase Z, β subunit: YES

Unification Links: DIP:DIP-10312N , EcoliWiki:b1225 , Mint:MINT-1260007 , ModBase:P11349 , PR:PRO_000023352 , Pride:P11349 , Protein Model Portal:P11349 , RefSeq:NP_415743 , SMR:P11349 , String:511145.b1225 , UniProt:P11349

Relationship Links: InterPro:IN-FAMILY:IPR006547 , InterPro:IN-FAMILY:IPR017896 , PDB:Structure:1Q16 , PDB:Structure:1R27 , PDB:Structure:1SIW , PDB:Structure:1Y4Z , PDB:Structure:1Y5I , PDB:Structure:1Y5L , PDB:Structure:1Y5N , PDB:Structure:3EGW , PDB:Structure:3IR5 , PDB:Structure:3IR6 , PDB:Structure:3IR7 , Pfam:IN-FAMILY:PF13247 , Prosite:IN-FAMILY:PS00198 , Prosite:IN-FAMILY:PS51379

Summary:
The β subunit (NarH) of nitrate reductase A contains 4 iron-sulfur clusters - one [3Fe-4S] cluster (FS4) and three [4Fe-4S] clusters (FS1, FS2 and FS3) [Johnson85, Blasco89, Bertero03]. FS1, FS2 and FS3 are coordinated by 4 cysteine residues and FS4 is coordinated by 3 cysteine residues (reviewed by [Blasco01]

nar: nitrate reductase; chl: chlorate resistant [Stewart82]

Citations: [Augier93, Augier93a, Guigliarelli96, Guigliarelli92]

Essentiality data for narH knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 2]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 3]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 4]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 3]
Yes [Feist07, Comment 5]

Subunit of nitrate reductase A: nitrate reductase A, γ subunit

Synonyms: ChlI, NarI

Gene: narI Accession Numbers: EG10640 (EcoCyc), b1227, ECK1221

Locations: inner membrane

Sequence Length: 225 AAs

Molecular Weight: 25.497 kD (from nucleotide sequence)

pI: 9.85

GO Terms:

Biological Process: GO:0009061 - anaerobic respiration Inferred from experiment [Sodergren88a]
GO:0042128 - nitrate assimilation Inferred by computational analysis [UniProtGOA11]
GO:0055114 - oxidation-reduction process Inferred by computational analysis [UniProtGOA11, GOA01]
Molecular Function: GO:0008940 - nitrate reductase activity Inferred from experiment Inferred by computational analysis [GOA01a, GOA01, Forget74, Rondeau84, Stewart82]
GO:0009055 - electron carrier activity Inferred from experiment [Bertero03, Rothery99]
GO:0020037 - heme binding Inferred from experiment [Rothery99, Magalon97a, Bertero03]
GO:0016491 - oxidoreductase activity Inferred by computational analysis [UniProtGOA11]
GO:0046872 - metal ion binding Inferred by computational analysis [UniProtGOA11]
Cellular Component: GO:0005886 - plasma membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11a, UniProtGOA11, DiazMejia09, Zhang07, Daley05]
GO:0005887 - integral component of plasma membrane Inferred by computational analysis Inferred from experiment [Bertero03, Berks95a]
GO:0009325 - nitrate reductase complex Inferred from experiment Inferred by computational analysis [GOA01, Sodergren88]
GO:0044799 - NarGHI complex Inferred from experiment [Bertero03, Forget74]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11]
GO:0016021 - integral component of membrane Inferred by computational analysis [UniProtGOA11]

MultiFun Terms: cell structure membrane
metabolism biosynthesis of macromolecules (cellular constituents) large molecule carriers cytochromes
metabolism energy metabolism, carbon anaerobic respiration
metabolism energy production/transport electron acceptors

Isozyme Sequence Similarity:
nitrate reductase Z, γ subunit: YES

Unification Links: DIP:DIP-10313N , EcoliWiki:b1227 , Mint:MINT-1262739 , ModBase:P11350 , PR:PRO_000023353 , Protein Model Portal:P11350 , RefSeq:NP_415745 , SMR:P11350 , String:511145.b1227 , UniProt:P11350

Relationship Links: InterPro:IN-FAMILY:IPR003816 , InterPro:IN-FAMILY:IPR023234 , PDB:Structure:1Q16 , PDB:Structure:1SIW , PDB:Structure:1Y4Z , PDB:Structure:1Y5I , PDB:Structure:1Y5L , PDB:Structure:1Y5N , PDB:Structure:3EGW , PDB:Structure:3IR5 , PDB:Structure:3IR6 , PDB:Structure:3IR7 , Pfam:IN-FAMILY:PF02665

Summary:
The γ subunit (NarI) of nitrate reductase A is a membrane-embedded heme-iron subunit resembling cytochrome b, which transfers electrons from the quinone pool to the β subunit (NarH). There are two hemes present, a low-potential heme bL and a high-potential heme bH [Hacket82, Magalon97a, Rothery99]. Electrons are thought to transfer from the quinol binding site (Q-site) via heme bL and heme bH to the [3Fe-4S] cluster of NarH [Magalon98, Rothery01a]. The Q-site of Nar is periplasmically oriented [Bertero05]. NarI contains 5 transmembrane helices; the first helix appears to facilitate dimer formation. A C-terminal tail interacts with both NarG and NarH. The two Fe atoms are coordinated by histidine groups - His 56 and His 205 coordinate heme bH, His66 and His 187 coordinate heme bL. NarI contains an elongated hydrophobic cavity which may provide a protected interaction site for quinones [Magalon97a, Bertero03].

Reviews: [Rothery01]

Citations: [MacGregor75a, Zhao03]

Essentiality data for narI knockouts: ?

Growth Medium Growth? T (°C) O2 pH Osm/L Growth Observations
LB enriched Yes 37 Aerobic 6.95   Yes [Gerdes03, Comment 2]
LB Lennox Yes 37 Aerobic 7   Yes [Baba06, Comment 3]
M9 medium with 1% glycerol Yes 37 Aerobic 7.2 0.35 Yes [Joyce06, Comment 4]
MOPS medium with 0.4% glucose Yes 37 Aerobic 7.2 0.22 Yes [Baba06, Comment 3]
Yes [Feist07, Comment 5]

References

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Augier93: Augier V, Guigliarelli B, Asso M, Bertrand P, Frixon C, Giordano G, Chippaux M, Blasco F (1993). "Site-directed mutagenesis of conserved cysteine residues within the beta subunit of Escherichia coli nitrate reductase. Physiological, biochemical, and EPR characterization of the mutated enzymes." Biochemistry 32(8);2013-23. PMID: 8383531

Augier93a: Augier V, Asso M, Guigliarelli B, More C, Bertrand P, Santini CL, Blasco F, Chippaux M, Giordano G (1993). "Removal of the high-potential [4Fe-4S] center of the beta-subunit from Escherichia coli nitrate reductase. Physiological, biochemical, and EPR characterization of site-directed mutated enzymes." Biochemistry 32(19);5099-108. PMID: 8388253

Avazeri97: Avazeri C, Turner RJ, Pommier J, Weiner JH, Giordano G, Vermeglio A (1997). "Tellurite reductase activity of nitrate reductase is responsible for the basal resistance of Escherichia coli to tellurite." Microbiology 143 ( Pt 4);1181-9. PMID: 9141681

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Blum82: Blum H, Poole RK (1982). "The molybdenum and iron-sulphur centres of Escherichia coli nitrate reductase are non-randomly oriented in the membrane." Biochem Biophys Res Commun 107(3);903-9. PMID: 6291520

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Butland05: Butland G, Peregrin-Alvarez JM, Li J, Yang W, Yang X, Canadien V, Starostine A, Richards D, Beattie B, Krogan N, Davey M, Parkinson J, Greenblatt J, Emili A (2005). "Interaction network containing conserved and essential protein complexes in Escherichia coli." Nature 433(7025);531-7. PMID: 15690043

Chan06: Chan CS, Howell JM, Workentine ML, Turner RJ (2006). "Twin-arginine translocase may have a role in the chaperone function of NarJ from Escherichia coli." Biochem Biophys Res Commun 343(1):244-51. PMID: 16540088

Chan09a: Chan CS, Chang L, Rommens KL, Turner RJ (2009). "Differential interactions between Tat-specific redox enzyme peptides and their chaperones." J Bacteriol 191(7):2091-101. PMID: 19151138

Chan10: Chan CS, Chang L, Winstone TM, Turner RJ (2010). "Comparing system-specific chaperone interactions with their Tat dependent redox enzyme substrates." FEBS Lett 584(22);4553-8. PMID: 20974141

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DiazMejia09: Diaz-Mejia JJ, Babu M, Emili A (2009). "Computational and experimental approaches to chart the Escherichia coli cell-envelope-associated proteome and interactome." FEMS Microbiol Rev 33(1);66-97. PMID: 19054114

Dubourdieu92: Dubourdieu M, DeMoss JA (1992). "The narJ gene product is required for biogenesis of respiratory nitrate reductase in Escherichia coli." J Bacteriol 1992;174(3);867-72. PMID: 1732220

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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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