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

Gene: frdC Accession Numbers: EG10332 (EcoCyc), b4152, ECK4148

Regulation Summary Diagram

Regulation summary diagram for frdC

Component of: fumarate reductase (extended summary available)

This is one of two integral membrane proteins in the four subunit fumarate reductase complex [Lemire82]. FrdC and FrdD each have three transmembrane helices connected by periplasmic loops; the N-terminus is located in the cytoplasm and the C-terminus is located in the periplasm. The transmembrane helices are positioned to form two menaquinone binding pockets [Iverson99]

Despite similar function, hydrophobicity, and protein size, the FrdC and FrdD subunits of fumarate reductase do not share significant sequence identity with the corresponding membrane-binding subunits of succinate dehydrogenase, SdhC and SdhD [Wood84].

Citations: [Westenberg93]

Gene Citations: [Tseng94, Tseng96]

Locations: inner membrane

Map Position: [4,377,400 <- 4,377,795] (94.35 centisomes, 340°)
Length: 396 bp / 131 aa

Molecular Weight of Polypeptide: 15.015 kD (from nucleotide sequence)

Unification Links: ASAP:ABE-0013598, CGSC:740, DIP:DIP-48082N, EchoBASE:EB0328, EcoGene:EG10332, EcoliWiki:b4152, Mint:MINT-1290104, ModBase:P0A8Q0, OU-Microarray:b4152, PortEco:frdC, PR:PRO_000022688, Protein Model Portal:P0A8Q0, RefSeq:NP_418576, RegulonDB:EG10332, SMR:P0A8Q0, String:511145.b4152, UniProt:P0A8Q0

Relationship Links: InterPro:IN-FAMILY:IPR003510, 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, Pfam:IN-FAMILY:PF02300, ProDom:IN-FAMILY:PD015900

Gene-Reaction Schematic

Gene-Reaction Schematic

Genetic Regulation Schematic

Genetic regulation schematic for frdC

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]
Inferred from experimentGO:0044780 - bacterial-type flagellum assembly [CohenBenLulu08]
Inferred by computational analysisGO:0006810 - transport [GOA00]
Molecular Function:
Inferred by computational analysisInferred from experimentGO:0000104 - succinate dehydrogenase activity [Lemire82, GOA01]
Inferred from experimentGO:0008177 - succinate dehydrogenase (ubiquinone) activity [Westenberg90]
Inferred by computational analysisGO:0016491 - oxidoreductase activity [GOA00, GOA01a]
Cellular Component:
Inferred from experimentInferred by computational analysisGO:0005886 - plasma membrane [UniProtGOA11, UniProtGOA11a, GOA06, DiazMejia09, Zhang07, Daley05]
Inferred from experimentGO:0045284 - plasma membrane fumarate reductase complex [Iverson99, Lemire82]
Inferred by computational analysisGO:0016020 - membrane [UniProtGOA11a, GOA01a]
Inferred by computational analysisGO:0016021 - integral component of membrane [UniProtGOA11a]

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

Essentiality data for frdC 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 [Spencer73a, 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, Johnson85, Johnson85a, 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, Jones87b, 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, Johnson85b, Salerno91, Lancaster00, Brandsch89, Tseng94, Kalman89, Kalman88, Goh05, Golby99, Latour88, Cecchini95, Rothery98, Cheng13, Manodori92, Kowal95, Singh13, Maklashina06, 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, Spencer73a, 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, Johnson85, Iverson99]
Inferred from experimentGO:0051538 - 3 iron, 4 sulfur cluster binding [Johnson85a, Iverson99]
Inferred from experimentGO:0051539 - 4 iron, 4 sulfur cluster binding [Johnson85, 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 [Maklashina06a, BRENDA14]
succinate 15.0 [Maklashina06, BRENDA14]
fumarate 5.4 177.0 32.78 [Cecchini02, BRENDA14]
fumarate 230.0 [Maklashina06, BRENDA14]
fumarate 20.0 250.0 12.5 [Maklashina06a, BRENDA14]

Sequence Features

Protein sequence of fumarate reductase membrane protein with features indicated

Feature Class Location Citations Comment
Pfam PF02300 3 -> 128
Inferred by computational analysis[Finn14]
Fumarate_red_C : Fumarate reductase subunit C
Transmembrane-Region 22 -> 49
Author statementInferred from experiment[UniProt10, Iverson99]
UniProt: Helical;
Transmembrane-Region 66 -> 90
Author statementInferred from experiment[UniProt10, Iverson99]
UniProt: Helical;
Transmembrane-Region 105 -> 128
Author statementInferred from experiment[UniProt10, Iverson99]
UniProt: Helical;

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

Gene local context diagram

Transcription Unit

Transcription-unit diagram


10/20/97 Gene b4152 from Blattner lab Genbank (v. M52) entry merged into EcoCyc gene EG10332; 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

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

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

Daley05: Daley DO, Rapp M, Granseth E, Melen K, Drew D, von Heijne G (2005). "Global topology analysis of the Escherichia coli inner membrane proteome." Science 308(5726);1321-3. PMID: 15919996

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

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."

GOA06: GOA, SIB (2006). "Electronic Gene Ontology annotations created by transferring manual GO annotations between orthologous microbial proteins."

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

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

Johnson85: 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

Johnson85a: 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

Johnson85b: 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

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

Jones87b: 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

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

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, 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

Maklashina06a: 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

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

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

Prasad98: Prasad K, Caplan SR, Eisenbach M (1998). "Fumarate modulates bacterial flagellar rotation by lowering the free energy difference between the clockwise and counterclockwise states of the motor." J Mol Biol 280(5);821-8. PMID: 9671552

Rothery05: Rothery RA, Seime AM, Spiers AM, Maklashina E, Schroder I, Gunsalus RP, Cecchini G, Weiner JH (2005). "Defining the Q-site of Escherichia coli fumarate reductase by site-directed mutagenesis, fluorescence quench titrations and EPR spectroscopy." FEBS J 272(2);313-26. PMID: 15654871

Rothery98: Rothery RA, Weiner JH (1998). "Interaction of a menaquinol binding site with the [3Fe-4S] cluster of Escherichia coli fumarate reductase." Eur J Biochem 254(3);588-95. PMID: 9688270

Salerno91: Salerno JC (1991). "Electron transfer in succinate:ubiquinone reductase and quinol:fumarate reductase." Biochem Soc Trans 19(3);599-605. PMID: 1664389

Singh13: Singh PK, Sarwar M, Maklashina E, Kotlyar V, Rajagukguk S, Tomasiak TM, Cecchini G, Iverson TM (2013). "Plasticity of the quinone-binding site of the complex II homolog quinol:fumarate reductase." J Biol Chem 288(34);24293-301. PMID: 23836905

Spencer73a: Spencer ME, Guest JR (1973). "Isolation and properties of fumarate reductase mutants of Escherichia coli." J Bacteriol 114(2);563-70. PMID: 4574693

Sucheta93: Sucheta A, Cammack R, Weiner J, Armstrong FA (1993). "Reversible electrochemistry of fumarate reductase immobilized on an electrode surface. Direct voltammetric observations of redox centers and their participation in rapid catalytic electron transport." Biochemistry 32(20);5455-65. PMID: 8499449

Tran97: Tran QH, Bongaerts J, Vlad D, Unden G (1997). "Requirement for the proton-pumping NADH dehydrogenase I of Escherichia coli in respiration of NADH to fumarate and its bioenergetic implications." Eur J Biochem 244(1);155-60. PMID: 9063459

Tseng94: Tseng CP, Hansen AK, Cotter P, Gunsalus RP (1994). "Effect of cell growth rate on expression of the anaerobic respiratory pathway operons frdABCD, dmsABC, and narGHJI of Escherichia coli." J Bacteriol 1994;176(21);6599-605. PMID: 7961411

Tseng96: Tseng CP, Albrecht J, Gunsalus RP (1996). "Effect of microaerophilic cell growth conditions on expression of the aerobic (cyoABCDE and cydAB) and anaerobic (narGHJI, frdABCD, and dmsABC) respiratory pathway genes in Escherichia coli." J Bacteriol 1996;178(4);1094-8. PMID: 8576043

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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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