Escherichia coli K-12 substr. MG1655 Polypeptide: fumarate reductase flavoprotein

Gene: frdA Accession Numbers: EG10330 (EcoCyc), b4154, ECK4150

Regulation Summary Diagram

Regulation summary diagram for frdA

Component of: fumarate reductase (extended summary available)

FrdA is one of two catalytic subunits in the four subunit fumarate reductase complex. This subunit contains the FAD cofactor [Weiner79, Cole82].

This protein has similarity to the SdhA subunit of succinate dehydrogenase [Wood84]. A 2.2 Å crystal structure of L-aspartate oxidase suggests that an unusual tertiary structure is shared by L-aspartate oxidase, the SdhA subunit of succinate dehydrogenase, and the FrdA subunit of fumarate reductase [Mattevi99].

Gene Citations: [Tseng94, Tseng96]

Locations: inner membrane, cytosol

Map Position: [4,380,510 <- 4,382,318] (94.37 centisomes, 340°)
Length: 1809 bp / 602 aa

Molecular Weight of Polypeptide: 65.972 kD (from nucleotide sequence), 69.0 kD (experimental) [Weiner79]

pI: 6.23

Unification Links: ASAP:ABE-0013604, CGSC:742, DIP:DIP-9681N, EchoBASE:EB0326, EcoGene:EG10330, EcoliWiki:b4154, Mint:MINT-1310079, ModBase:P00363, OU-Microarray:b4154, PortEco:frdA, PR:PRO_000022686, Pride:P00363, Protein Model Portal:P00363, RefSeq:NP_418578, RegulonDB:EG10330, SMR:P00363, String:511145.b4154, UniProt:P00363

Relationship Links: InterPro:IN-FAMILY:IPR003952, InterPro:IN-FAMILY:IPR003953, InterPro:IN-FAMILY:IPR005884, InterPro:IN-FAMILY:IPR014006, InterPro:IN-FAMILY:IPR015939, InterPro:IN-FAMILY:IPR027477, Panther:IN-FAMILY:PTHR11632:SF5, PDB:Structure:1KF6, PDB:Structure:1KFY, PDB:Structure:1L0V, PDB:Structure:2B76, PDB:Structure:3CIR, PDB:Structure:3P4P, PDB:Structure:3P4Q, PDB:Structure:3P4R, PDB:Structure:3P4S, PDB:Structure:4KX6, Pfam:IN-FAMILY:PF00890, Pfam:IN-FAMILY:PF02910, Prints:IN-FAMILY:PR00368, Prosite:IN-FAMILY:PS00504

In Paralogous Gene Group: 434 (3 members)

Gene-Reaction Schematic

Gene-Reaction Schematic

Genetic Regulation Schematic

Genetic regulation schematic for frdA

GO Terms:
Biological Process:
Inferred from experimentGO:0001539 - cilium or flagellum-dependent cell motility [CohenBenLulu08]
Inferred from experimentGO:0006113 - fermentation [Hirsch63]
Inferred from experimentGO:0006974 - cellular response to DNA damage stimulus [Khil02]
Inferred from experimentInferred by computational analysisGO:0009061 - anaerobic respiration [GOA01a, Condon88, Hirsch63]
Inferred from experimentGO:0044780 - bacterial-type flagellum assembly [CohenBenLulu08]
Inferred by computational analysisGO:0022900 - electron transport chain [GOA01a]
Inferred by computational analysisGO:0055114 - oxidation-reduction process [UniProtGOA11a, GOA01a]
Molecular Function:
Inferred from experimentGO:0000104 - succinate dehydrogenase activity [Lemire82]
Inferred from experimentGO:0005515 - protein binding [Huang06a, Lasserre06, Iverson02]
Inferred from experimentGO:0009055 - electron carrier activity [Leger01, Sucheta93]
Inferred by computational analysisInferred from experimentGO:0071949 - FAD binding [Weiner79, Cole82]
Inferred by computational analysisGO:0016491 - oxidoreductase activity [UniProtGOA11a, GOA01a]
Inferred by computational analysisGO:0016627 - oxidoreductase activity, acting on the CH-CH group of donors [GOA01a]
Inferred by computational analysisGO:0050660 - flavin adenine dinucleotide binding [GOA01a]
Cellular Component:
Inferred from experimentGO:0005829 - cytosol [Lemire82, Iverson99]
Inferred from experimentGO:0016020 - membrane [Lasserre06]
Inferred from experimentGO:0045284 - plasma membrane fumarate reductase complex [Iverson99, Lemire82]

MultiFun Terms: metabolismenergy metabolism, carbonanaerobic respiration
metabolismenergy metabolism, carbonfermentation
metabolismenergy production/transportelectron acceptors

Essentiality data for frdA knockouts:

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

Last-Curated 28-Apr-2008 by Nolan L, Macquarie University

Subunit of: fumarate reductase

Synonyms: menaquinol:fumarate oxidoreductase, FRD, QFR, fumarate reductase, quinol:fumarate oxidoreductase

Subunit composition of fumarate reductase = [FrdA][FrdB][FrdC][FrdD]
         fumarate reductase flavoprotein = FrdA (summary available)
         fumarate reductase iron-sulfur protein = FrdB (summary available)
         fumarate reductase membrane protein = FrdC (summary available)
         fumarate reductase membrane protein = FrdD (summary available)

Quinol:fumarate oxidoreductase (QFR) or fumarate reductase or is a membrane bound flavoprotein that catalyses the reduction of fumarate to succinate under anaerobic conditions [Hirsch63]. QFR is a respiratory enzyme - it is one of a number of reductases that function as terminal electron acceptors during anaerobic respiration in E. coli K-12 (reviewed by [Unden97].

Functional QFR is essential for anaerobic growth on glycerol, lactate or formate when fumarate serves as the terminal electron acceptor. It is also essential for anaerobic H2 dependent growth with fumarate. Menaquinone is the obligatory electron donor [Spencer73, Lambden76, Wissenbach90]. Anaerobic growth of E. coli K-12 with fumarate operates preferentially with NADH dehydrogenase I [Tran97]

Fumarate reductase is composed of 4 subunits; the complex contains a cytoplasmic catalytic domain - FrdAB - containing bound flavin cofactor and three iron-sulfur clusters and a membrane anchor domain (FrdCD) which contains the quinol binding site(s) [Weiner79, Lohmeier81, Lemire82, Morningstar85, Johnson85b, Johnson85c, Iverson99]. All 4 subunits are essential for anaerobic growth on glycerol and fumarate [Condon88]. The crystal structure of purified fumarate reductase contains two menaquinol molecules (Qp and Qd) bound on opposite sides of the membrane-spanning region; Qp is proximal to the site of fumarate reduction, Qd is distal. It is not clear whether both of the quinol-binding sites are functionally relevant [Iverson99, Iverson02, Iverson00, Rothery05]. The 6 redox cofactors are organised in a chain with the sequence FAD - 2Fe:2S - 4Fe:4S - 3Fe:4S - Qp - Qd [Iverson99].

QFR is structurally and functionally homologous to succinate dehydrogenase (SQR) which catalyses the oxidation of succinate to fumarate under aerobic conditions. The functions of QFR and SQR are partially interchangeable - a plasmid containing the frd genes is able to compensate for the growth deficiency of an sdh mutant [Guest81] while anaerobic expression of succinate dehydrogenase supports the growth of an frd mutant [Maklashina98].

A crystal structure of the purified complex indicated dimer formation but this is unlikely to be physiologically relevent [Iverson99].

Expression of the frd operon is repressed by the preferred electron acceptors, oxygen and nitrate and induced by fumarate [Jones85, Jones87a, Iuchi87].

QFR transmits the effects of fumarate (known to be a flagella switching factor in E. coli [Barak96, Prasad98]) to the flagella switch. Cells lacking QFR are defective in flagella assembly and switching of flagella rotation as well as being insensitive to fumarate. QFR interacts with the flagella switch protein FliG in vitro [CohenBenLulu08].

Reviews: [Cecchini02]
Comment: [Hederstedt99]

Citations: [Cole85, Guest79, Johnson85a, Salerno91, Lancaster00, Brandsch89, Tseng94, Kalman89, Kalman88, Goh05, Golby99, Latour88, Cecchini95, Rothery98a, Cheng13, Manodori92, Kowal95, Singh13a, Maklashina06a, Dickie79, vanderPlas83]

Locations: inner membrane

Relationship Links: PDB:Structure:1KF6, PDB:Structure:1KFY, PDB:Structure:1L0V

GO Terms:
Biological Process:
Inferred from experimentGO:0001539 - cilium or flagellum-dependent cell motility [CohenBenLulu08]
Inferred from experimentGO:0006113 - fermentation [Hirsch63]
Inferred from experimentGO:0009061 - anaerobic respiration [Condon88, Hirsch63, Spencer73, Lambden76]
Inferred from experimentGO:0019645 - anaerobic electron transport chain [Miki75]
Inferred from experimentGO:0044780 - bacterial-type flagellum assembly [CohenBenLulu08]
Molecular Function:
Inferred by computational analysisInferred from experimentGO:0000104 - succinate dehydrogenase activity [Lemire82, Hirsch63, GOA01]
Inferred from experimentGO:0005515 - protein binding [CohenBenLulu08]
Inferred from experimentGO:0008177 - succinate dehydrogenase (ubiquinone) activity [Lambden76]
Inferred from experimentGO:0009055 - electron carrier activity [Leger01, Sucheta93]
Inferred from experimentGO:0051537 - 2 iron, 2 sulfur cluster binding [Morningstar85, Johnson85b, Iverson99]
Inferred from experimentGO:0051538 - 3 iron, 4 sulfur cluster binding [Johnson85c, Iverson99]
Inferred from experimentGO:0051539 - 4 iron, 4 sulfur cluster binding [Johnson85b, Iverson99]
Inferred from experimentGO:0071949 - FAD binding [Weiner79]
Inferred by computational analysisGO:0016491 - oxidoreductase activity [GOA00, GOA01a]
Cellular Component:
Inferred from experimentGO:0005887 - integral component of plasma membrane [Lemire82]
Inferred from experimentGO:0045284 - plasma membrane fumarate reductase complex [Iverson99, Lemire82]

Revised 27-Aug-2014 by Mackie A, Macquarie University
Last-Curated 27-Aug-2014 by Mackie A, Macquarie University

Enzymatic reaction of: fumarate reductase

Inferred from experiment

Synonyms: QFR, menaquinol-fumarate oxidoreductase, FrdABCD, fumarate reductase

EC Number:

Transport reaction diagram for fumarate reductase

In Pathways: mixed acid fermentation, NADH to fumarate electron transfer, hydrogen to fumarate electron transfer, glycerol-3-phosphate to fumarate electron transfer

Citations: [LunaChavez00, Cole85]

Cofactors or Prosthetic Groups: a [2Fe-2S] iron-sulfur cluster, a [3Fe-4S] iron-sulfur cluster, a [4Fe-4S] iron-sulfur cluster, FAD

Inhibitors (Competitive): malonate [Maklashina99], a 2-alkyl-dinitrophenol derivative [Comment 5], a ubiquinol analogue [Comment 6], pentachlorophenol [Maklashina99] Inhibitors (Noncompetitive): a 2-alkyl-dinitrophenol derivative [Maklashina99, Comment 7], 2-n-heptyl-4-hydroxyquinoline-N-oxide [Maklashina99] Inhibitors (Unknown Mechanism): oxaloacetate [Iverson99]

Primary Physiological Regulators of Enzyme Activity: oxaloacetate, malonate

Kinetic Parameters:
Substrate Km (μM) kcat (sec-1) kcat/Km (sec-1 μM-1) Citations
succinate 1.5 14.0 9.33 [Cecchini02, BRENDA14]
succinate 550.0 30.0 0.055 [Maklashina06, BRENDA14]
succinate 15.0 [Maklashina06a, BRENDA14]
fumarate 5.4 177.0 32.78 [Cecchini02, BRENDA14]
fumarate 230.0 [Maklashina06a, BRENDA14]
fumarate 20.0 250.0 12.5 [Maklashina06, BRENDA14]

Sequence Features

Protein sequence of fumarate reductase flavoprotein with features indicated

Feature Class Location Attached Group Citations Comment
Cleavage-of-Initial-Methionine 1  
Author statement[UniProt15]
UniProt: Removed.
Chain 2 -> 602  
Author statement[UniProt15]
UniProt: Fumarate reductase flavoprotein subunit.
Nucleotide-Phosphate-Binding-Region 9 -> 23 FAD
Inferred by computational analysis[UniProt15]
UniProt: FAD.
Mutagenesis-Variant 45  
Inferred from experiment[Blaut89]
Inferred from experiment[Blaut89]
H → C, S or Y: Decreased ability (greater than 70%) to reduce fumarate.
H → R: Inactivates enzyme.
Tele-8alpha-FAD-histidine-Modification 45  
Author statementInferred by computational analysis[UniProt11a, Cole82]
UniProt: Tele-8alpha-FAD histidine.
Mutagenesis-Variant 233  
Inferred from experiment[Schroder91]
UniProt: Severely affect succinate oxidation and decrease fumarate oxidation by 75%.
Active-Site 233  
Author statement[UniProt15]
Mutagenesis-Variant 248  
Inferred from experiment[Schroder91]
C → A or S: Does not inactivate enzyme.
Mutagenesis-Variant 249  
Inferred from experiment[Schroder91]
R → H or L: Inactivates enzyme.
Active-Site 249  
Author statement[UniProt15]
Sequence-Conflict 386  
Inferred by curator[Cole82, UniProt15]
UniProt: (in Ref. 1; AAA23437).

Sequence Pfam Features

Protein sequence of fumarate reductase flavoprotein with features indicated

Feature Class Location Citations Comment
Pfam PF00890 7 -> 397
Inferred by computational analysis[Finn14]
FAD_binding_2 : FAD binding domain [More...]
Pfam PF02910 453 -> 581
Inferred by computational analysis[Finn14]
Succ_DH_flav_C : Fumarate reductase flavoprotein C-term [More...]

Gene Local Context (not to scale -- see Genome Browser for correct scale)

Transcription Unit

Transcription-unit diagram


10/20/97 Gene b4154 from Blattner lab Genbank (v. M52) entry merged into EcoCyc gene EG10330; confirmed by SwissProt match.


Baba06: Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, Mori H (2006). "Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection." Mol Syst Biol 2;2006.0008. PMID: 16738554

Barak96: Barak R, Giebel I, Eisenbach M (1996). "The specificity of fumarate as a switching factor of the bacterial flagellar motor." Mol Microbiol 19(1);139-44. PMID: 8821943

Blaut89: Blaut M, Whittaker K, Valdovinos A, Ackrell BA, Gunsalus RP, Cecchini G (1989). "Fumarate reductase mutants of Escherichia coli that lack covalently bound flavin." J Biol Chem 264(23);13599-604. PMID: 2668268

Brandsch89: Brandsch R, Bichler V (1989). "Covalent cofactor binding to flavoenzymes requires specific effectors." Eur J Biochem 1989;182(1);125-8. PMID: 2659351

BRENDA14: BRENDA team (2014). Imported from BRENDA version existing on Aug 2014.

Cecchini02: Cecchini G, Schroder I, Gunsalus RP, Maklashina E (2002). "Succinate dehydrogenase and fumarate reductase from Escherichia coli." Biochim Biophys Acta 1553(1-2);140-57. PMID: 11803023

Cecchini86: Cecchini G, Thompson CR, Ackrell BA, Westenberg DJ, Dean N, Gunsalus RP (1986). "Oxidation of reduced menaquinone by the fumarate reductase complex in Escherichia coli requires the hydrophobic FrdD peptide." Proc Natl Acad Sci U S A 83(23);8898-902. PMID: 3538014

Cecchini95: Cecchini G, Sices H, Schroder I, Gunsalus RP (1995). "Aerobic inactivation of fumarate reductase from Escherichia coli by mutation of the [3Fe-4S]-quinone binding domain." J Bacteriol 177(16);4587-92. PMID: 7642483

Cheng13: Cheng VW, Tran QM, Boroumand N, Rothery RA, Maklashina E, Cecchini G, Weiner JH (2013). "A conserved lysine residue controls iron-sulfur cluster redox chemistry in Escherichia coli fumarate reductase." Biochim Biophys Acta 1827(10);1141-7. PMID: 23711795

CohenBenLulu08: Cohen-Ben-Lulu GN, Francis NR, Shimoni E, Noy D, Davidov Y, Prasad K, Sagi Y, Cecchini G, Johnstone RM, Eisenbach M (2008). "The bacterial flagellar switch complex is getting more complex." EMBO J 27(7);1134-44. PMID: 18337747

Cole82: Cole ST (1982). "Nucleotide sequence coding for the flavoprotein subunit of the fumarate reductase of Escherichia coli." Eur J Biochem 122(3);479-84. PMID: 7037404

Cole85: Cole ST, Condon C, Lemire BD, Weiner JH (1985). "Molecular biology, biochemistry and bioenergetics of fumarate reductase, a complex membrane-bound iron-sulfur flavoenzyme of Escherichia coli." Biochim Biophys Acta 1985;811(4);381-403. PMID: 3910107

Condon88: Condon C, Weiner JH (1988). "Fumarate reductase of Escherichia coli: an investigation of function and assembly using in vivo complementation." Mol Microbiol 2(1);43-52. PMID: 3285122

Dickie79: Dickie P, Weiner JH (1979). "Purification and characterization of membrane-bound fumarate reductase from anaerobically grown Escherichia coli." Can J Biochem 57(6);813-21. PMID: 383238

Feist07: Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, Palsson BO (2007). "A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information." Mol Syst Biol 3;121. PMID: 17593909

Finn14: Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M (2014). "Pfam: the protein families database." Nucleic Acids Res 42(Database issue);D222-30. PMID: 24288371

Gerdes03: Gerdes SY, Scholle MD, Campbell JW, Balazsi G, Ravasz E, Daugherty MD, Somera AL, Kyrpides NC, Anderson I, Gelfand MS, Bhattacharya A, Kapatral V, D'Souza M, Baev MV, Grechkin Y, Mseeh F, Fonstein MY, Overbeek R, Barabasi AL, Oltvai ZN, Osterman AL (2003). "Experimental determination and system level analysis of essential genes in Escherichia coli MG1655." J Bacteriol 185(19);5673-84. PMID: 13129938

GOA00: GOA (2000). "Gene Ontology annotation based on Swiss-Prot keyword mapping."

GOA01: GOA, MGI (2001). "Gene Ontology annotation based on Enzyme Commission mapping." Genomics 74;121-128.

GOA01a: GOA, DDB, FB, MGI, ZFIN (2001). "Gene Ontology annotation through association of InterPro records with GO terms."

Goh05: Goh EB, Bledsoe PJ, Chen LL, Gyaneshwar P, Stewart V, Igo MM (2005). "Hierarchical control of anaerobic gene expression in Escherichia coli K-12: the nitrate-responsive NarX-NarL regulatory system represses synthesis of the fumarate-responsive DcuS-DcuR regulatory system." J Bacteriol 187(14);4890-9. PMID: 15995204

Golby99: Golby P, Davies S, Kelly DJ, Guest JR, Andrews SC (1999). "Identification and characterization of a two-component sensor-kinase and response-regulator system (DcuS-DcuR) controlling gene expression in response to C4-dicarboxylates in Escherichia coli." J Bacteriol 1999;181(4);1238-48. PMID: 9973351

Grundstrom80: Grundstrom T, Jaurin B, Edlund T, Normark S (1980). "Physical mapping and expression of hybrid plasmids carrying chromosomal beta-lactamase genes of Escherichia coli K-12." J Bacteriol 143(3);1127-34. PMID: 6251026

Guest79: Guest JR (1979). "Anaerobic growth of Escherichia coli K12 with fumarate as terminal electron acceptor. Genetic studies with menaquinone and fluoroacetate-resistant mutants." J Gen Microbiol 115(2);259-71. PMID: 393800

Guest81: Guest JR (1981). "Partial replacement of succinate dehydrogenase function by phage- and plasmid-specified fumarate reductase in Escherichia coli." J Gen Microbiol 122(Pt 2);171-9. PMID: 6274999

Hederstedt99: Hederstedt L (1999). "Respiration without O2." Science 284(5422);1941-2. PMID: 10400536

Hirsch63: Hirsch CA, Rasminsky M, Davis BD, Lin EC (1963). "A fumarate reductase in Escherichia coli distinct from succinate dehydrogenase." J Biol Chem 238;3770-4. PMID: 14109218

Huang06a: Huang CZ, Lin XM, Wu LN, Zhang DF, Liu D, Wang SY, Peng XX (2006). "Systematic identification of the subproteome of Escherichia coli cell envelope reveals the interaction network of membrane proteins and membrane-associated peripheral proteins." J Proteome Res 5(12);3268-76. PMID: 17137328

Iuchi87: Iuchi S, Lin EC (1987). "The narL gene product activates the nitrate reductase operon and represses the fumarate reductase and trimethylamine N-oxide reductase operons in Escherichia coli." Proc Natl Acad Sci U S A 1987;84(11);3901-5. PMID: 3035558

Iverson00: Iverson TM, Luna-Chavez C, Schroder I, Cecchini G, Rees DC (2000). "Analyzing your complexes: structure of the quinol-fumarate reductase respiratory complex." Curr Opin Struct Biol 10(4);448-55. PMID: 10981634

Iverson02: Iverson TM, Luna-Chavez C, Croal LR, Cecchini G, Rees DC (2002). "Crystallographic studies of the Escherichia coli quinol-fumarate reductase with inhibitors bound to the quinol-binding site." J Biol Chem 277(18);16124-30. PMID: 11850430

Iverson99: Iverson TM, Luna-Chavez C, Cecchini G, Rees DC (1999). "Structure of the Escherichia coli fumarate reductase respiratory complex." Science 1999;284(5422);1961-6. PMID: 10373108

Johnson85a: Johnson MK, Bennett DE, Morningstar JE, Adams MW, Mortenson LE (1985). "The iron-sulfur cluster composition of Escherichia coli nitrate reductase." J Biol Chem 260(9);5456-63. PMID: 2985594

Johnson85b: Johnson MK, Morningstar JE, Cecchini G, Ackrell BA (1985). "Detection of a tetranuclear iron-sulfur center in fumarate reductase from Escherichia coli by electron paramagnetic resonance spectroscopy." Biochem Biophys Res Commun 131(2);756-62. PMID: 2996525

Johnson85c: Johnson MK, Morningstar JE, Cecchini G, Ackrell BA (1985). "In vivo detection of a three iron cluster in fumarate reductase from Escherichia coli." Biochem Biophys Res Commun 131(2);653-8. PMID: 2996520

Jones85: Jones HM, Gunsalus RP (1985). "Transcription of the Escherichia coli fumarate reductase genes (frdABCD) and their coordinate regulation by oxygen, nitrate, and fumarate." J Bacteriol 1985;164(3);1100-9. PMID: 2999070

Jones87a: Jones HM, Gunsalus RP (1987). "Regulation of Escherichia coli fumarate reductase (frdABCD) operon expression by respiratory electron acceptors and the fnr gene product." J Bacteriol 169(7);3340-9. PMID: 3298218

Joyce06: Joyce AR, Reed JL, White A, Edwards R, Osterman A, Baba T, Mori H, Lesely SA, Palsson BO, Agarwalla S (2006). "Experimental and computational assessment of conditionally essential genes in Escherichia coli." J Bacteriol 188(23);8259-71. PMID: 17012394

Kalman88: Kalman LV, Gunsalus RP (1988). "The frdR gene of Escherichia coli globally regulates several operons involved in anaerobic growth in response to nitrate." J Bacteriol 170(2);623-9. PMID: 3276662

Kalman89: Kalman LV, Gunsalus RP (1989). "Identification of a second gene involved in global regulation of fumarate reductase and other nitrate-controlled genes for anaerobic respiration in Escherichia coli." J Bacteriol 171(7);3810-6. PMID: 2544557

Khil02: Khil PP, Camerini-Otero RD (2002). "Over 1000 genes are involved in the DNA damage response of Escherichia coli." Mol Microbiol 44(1);89-105. PMID: 11967071

Kowal95: Kowal AT, Werth MT, Manodori A, Cecchini G, Schroder I, Gunsalus RP, Johnson MK (1995). "Effect of cysteine to serine mutations on the properties of the [4Fe-4S] center in Escherichia coli fumarate reductase." Biochemistry 34(38);12284-93. PMID: 7547971

Lambden76: Lambden PR, Guest JR (1976). "Mutants of Escherichia coli K12 unable to use fumarate as an anaerobic electron acceptor." J Gen Microbiol 1976;97(2);145-60. PMID: 796407

Lancaster00: Lancaster CR, Kroger A (2000). "Succinate: quinone oxidoreductases: new insights from X-ray crystal structures." Biochim Biophys Acta 1459(2-3);422-31. PMID: 11004459

Lasserre06: Lasserre JP, Beyne E, Pyndiah S, Lapaillerie D, Claverol S, Bonneu M (2006). "A complexomic study of Escherichia coli using two-dimensional blue native/SDS polyacrylamide gel electrophoresis." Electrophoresis 27(16);3306-21. PMID: 16858726

Latour88: Latour DJ, Weiner JH (1988). "Regulation of in vitro expression of the Escherichia coli frd operon: alanine and Fnr represent positive and negative control elements." Nucleic Acids Res 16(14A);6339-52. PMID: 2456525

Leger01: Leger C, Heffron K, Pershad HR, Maklashina E, Luna-Chavez C, Cecchini G, Ackrell BA, Armstrong FA (2001). "Enzyme electrokinetics: energetics of succinate oxidation by fumarate reductase and succinate dehydrogenase." Biochemistry 40(37);11234-45. PMID: 11551223

Lemire82: Lemire BD, Robinson JJ, Weiner JH (1982). "Identification of membrane anchor polypeptides of Escherichia coli fumarate reductase." J Bacteriol 152(3);1126-31. PMID: 6754697

Lohmeier81: Lohmeier E, Hagen DS, Dickie P, Weiner JH (1981). "Cloning and expression of fumarate reductase gene of Escherichia coli." Can J Biochem 59(3);158-64. PMID: 7013950

LunaChavez00: Luna-Chavez C, Iverson TM, Rees DC, Cecchini G (2000). "Overexpression, purification, and crystallization of the membrane-bound fumarate reductase from Escherichia coli." Protein Expr Purif 2000;19(1);188-96. PMID: 10833406

Maklashina06: Maklashina E, Iverson TM, Sher Y, Kotlyar V, Andrell J, Mirza O, Hudson JM, Armstrong FA, Rothery RA, Weiner JH, Cecchini G (2006). "Fumarate reductase and succinate oxidase activity of Escherichia coli complex II homologs are perturbed differently by mutation of the flavin binding domain." J Biol Chem 281(16);11357-65. PMID: 16484232

Maklashina06a: Maklashina E, Hellwig P, Rothery RA, Kotlyar V, Sher Y, Weiner JH, Cecchini G (2006). "Differences in protonation of ubiquinone and menaquinone in fumarate reductase from Escherichia coli." J Biol Chem 281(36);26655-64. PMID: 16829675

Maklashina98: Maklashina E, Berthold DA, Cecchini G (1998). "Anaerobic expression of Escherichia coli succinate dehydrogenase: functional replacement of fumarate reductase in the respiratory chain during anaerobic growth." J Bacteriol 180(22);5989-96. PMID: 9811659

Maklashina99: Maklashina E, Cecchini G (1999). "Comparison of catalytic activity and inhibitors of quinone reactions of succinate dehydrogenase (Succinate-ubiquinone oxidoreductase) and fumarate reductase (Menaquinol-fumarate oxidoreductase) from Escherichia coli." Arch Biochem Biophys 1999;369(2);223-32. PMID: 10486141

Manodori92: Manodori A, Cecchini G, Schroder I, Gunsalus RP, Werth MT, Johnson MK (1992). "[3Fe-4S] to [4Fe-4S] cluster conversion in Escherichia coli fumarate reductase by site-directed mutagenesis." Biochemistry 31(10);2703-12. PMID: 1312345

Mattevi99: Mattevi A, Tedeschi G, Bacchella L, Coda A, Negri A, Ronchi S (1999). "Structure of L-aspartate oxidase: implications for the succinate dehydrogenase/fumarate reductase oxidoreductase family." Structure Fold Des 7(7);745-56. PMID: 10425677

Miki75: Miki K, Lin EC (1975). "Anaerobic energy-yielding reaction associated with transhydrogenation from glycerol 3-phosphate to fumarate by an Escherichia coli system." J Bacteriol 124(3);1282-7. PMID: 127785

Morningstar85: Morningstar JE, Johnson MK, Cecchini G, Ackrell BA, Kearney EB (1985). "The high potential iron-sulfur center in Escherichia coli fumarate reductase is a three-iron cluster." J Biol Chem 260(25);13631-8. PMID: 2997176

Park06: Park YJ, Yoo CB, Choi SY, Lee HB (2006). "Purifications and characterizations of a ferredoxin and its related 2-oxoacid:ferredoxin oxidoreductase from the hyperthermophilic archaeon, Sulfolobus solfataricus P1." J Biochem Mol Biol 39(1);46-54. PMID: 16466637

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Other References Related to Gene Regulation

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ShalelLevanon05: Shalel-Levanon S, San KY, Bennett GN (2005). "Effect of ArcA and FNR on the expression of genes related to the oxygen regulation and the glycolysis pathway in Escherichia coli under microaerobic growth conditions." Biotechnol Bioeng 92(2):147-59. PMID: 15988767

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Zientz98: Zientz E, Bongaerts J, Unden G (1998). "Fumarate regulation of gene expression in Escherichia coli by the DcuSR (dcuSR genes) two-component regulatory system." J Bacteriol 1998;180(20);5421-5. PMID: 9765574

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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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