Escherichia coli K-12 substr. MG1655 Polypeptide: TolR

Gene: tolR Accession Numbers: EG11011 (EcoCyc), b0738, ECK0727

Regulation Summary Diagram: ?

Regulation summary diagram for tolR

Component of: The Tol-Pal Cell Envelope Complex (extended summary available)

TolR is one of three (along with TolA and TolQ) inner membrane protein members of the YbgC-YbgF-TolQ-R-A-B-Pal Cell Envelope Complex, also known as the Tol-Pal system. The inner membrane protein, TolA, forms a transmembrane link with the outer membrane lipoprotein, Pal, in an energy-dependent manner [Cascales00]. The Tol-Pal system functions to maintain cell envelope integrity and also serves a role in the import of group A colicins and DNA of filamentous bacteria.

TolA, TolQ, and TolR interact with each other in the cytoplasmic membrane and are homologous to the TonB, ExbB and ExbD complex which uses proton motive force (pmf) to drive uptake through the bacterial outer membrane [Cascales01]. Deletion mutation studies indicate that TolR is essential for TolA-Pal complex interaction [Cascales01]. Organisation of the TolR transmembrane helices has been studied using cysteine substitution mutageneisis [Zhang09]

tolR is located in an operon encoding YbgCF-TolQRAB-Pal proteins [Walburger02].

Review: [Lazzaroni02].

Gene Citations: [Vianney96]

Locations: inner membrane

Map Position: [775,072 -> 775,500] (16.71 centisomes, 60°)
Length: 429 bp / 142 aa

Molecular Weight of Polypeptide: 15.383 kD (from nucleotide sequence)

Unification Links: ASAP:ABE-0002513 , CGSC:17812 , DIP:DIP-48143N , EchoBASE:EB1004 , EcoGene:EG11011 , EcoliWiki:b0738 , OU-Microarray:b0738 , PortEco:tolR , PR:PRO_000024082 , Protein Model Portal:P0ABV6 , RefSeq:NP_415266 , RegulonDB:EG11011 , SMR:P0ABV6 , String:511145.b0738 , UniProt:P0ABV6

Relationship Links: InterPro:IN-FAMILY:IPR003400 , InterPro:IN-FAMILY:IPR014168 , Pfam:IN-FAMILY:PF02472

Gene-Reaction Schematic: ?

Gene-Reaction Schematic

GO Terms:

Biological Process: GO:0043213 - bacteriocin transport Inferred from experiment Inferred by computational analysis [UniProtGOA11a, Goemaere07]
GO:0006810 - transport Inferred by computational analysis [UniProtGOA11a, GOA01a]
GO:0015031 - protein transport Inferred by computational analysis [UniProtGOA11a, GOA01a]
Molecular Function: GO:0005215 - transporter activity Inferred by computational analysis [GOA01a]
Cellular Component: GO:0005886 - plasma membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11, UniProtGOA11a, DiazMejia09, Kampfenkel93]
GO:0016021 - integral component of membrane Inferred from experiment Inferred by computational analysis [UniProtGOA11a, GOA01a, Kampfenkel93]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11a, GOA01a]

MultiFun Terms: cell structure membrane
extrachromosomal prophage genes and phage related functions

Essentiality data for tolR knockouts: ?

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

Subunit of: The Tol-Pal Cell Envelope Complex

Subunit composition of The Tol-Pal Cell Envelope Complex = [TolA][TolQ][TolR][TolB][CpoB][Pal]
         predicted periplasmic protein = CpoB (summary available)

The Tol-Pal system of the Escherichia coli cell envelope is made up of six proteins. These system proteins are encoded by genes organized into two operons. The first encodes YbgC, TolQ, TolR, TolA, TolB, Pal and YbgF and the second from an inner promoter encodes TolB, Pal and YbgF [Walburger02]. TolQ, TolR and TolA complex together in the inner membrane [Derouiche95], while TolB, a periplasmic protein, interacts with peptidoglycan-associated lipoprotein, Pal, which is anchored to the outer membrane and with the C-terminal domain of TolA [Walburger02]. TolB has also been shown to interact in vivo with the major outer membrane lipoprotein (Lpp) and OmpA in a Pal-dependent manner [Clavel98]. In addition, purified TolB was shown to interact with the trimeric porins OmpF, OmpC, PhoE, and LamB [Rigal97]. YbgC is a cytoplasmic acyl-ACP thioesterase involved in phospholipid metabolism [Gully06]. YbgF is a periplasmic protein which interacts with the central domain of TolA [Walburger02]. Studies have shown that tol-pal system mutants display hypersensitivity to drugs and detergents [Davies75], [Cascales00], allow for the pleiotropic release of periplasmic proteins [FogniniLefebvre87], and form outer membrane vesicles containing trimeric porins correctly exposed at the cell surface [Bernadac98]. These results give strong evidence that the Tol/Pal system functions to maintain cell envelope integrity [Walburger02]. Mapping of interactive regions of the subcomponents of the Tol-Pal system indicate that TolA, TolB and TolR all map within the colicin A N-terminal domain [Journet01], indicating that multiple contacts with the Tol/Pal system periplasmic proteins are required for group A colicin toxin uptake. The Tol proteins function to maintain the colicins in an unfolded conformation, aiding in their translocation across the periplasm and targeting to the cytoplasmic membrane or cytoplasm [Lazdunski98]. The Tol-Pal system is also implicated in filamentous phage infection [Click97]. While initial bacterial membrane-phage interaction occurs between the phage gene III protein (pIII) and the bacterial F-pilus [Sun86], subsequent integration of the phage capsid and concomitant DNA translocation into the cytoplasm occurs through a process primarily involving TolA [Click97, Karlsson03] Studies using protonophores indicate that the interaction between TolA and the Pal lipoprotein form a link between the inner and outer membrane and that this interaction is driven by the membrane proton motive force (pmf) [Cascales00]. Sequence analysis indicates that TolQ and TolR share structural and functional homologies with ExbB and ExbD of the TonB system as well as with MotA and MotB of the flagellar motor system, both of which are ion potential-driven molecular motor systems [Cascales01].

Sequence Features

Protein sequence of TolR with features indicated

Feature Class Location Citations Comment
Transmembrane-Region 21 -> 40
UniProt: Helical; Signal-anchor for type II membrane protein;; Non-Experimental Qualifier: probable;

Gene Local Context (not to scale): ?

Gene local context diagram

Transcription Units:

Transcription-unit diagram

Transcription-unit diagram


10/20/97 Gene b0738 from Blattner lab Genbank (v. M52) entry merged into EcoCyc gene EG11011; 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

Bernadac98: Bernadac A, Gavioli M, Lazzaroni JC, Raina S, Lloubes R (1998). "Escherichia coli tol-pal mutants form outer membrane vesicles." J Bacteriol 180(18);4872-8. PMID: 9733690

Cascales00: Cascales E, Gavioli M, Sturgis JN, Lloubes R (2000). "Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli." Mol Microbiol 38(4);904-15. PMID: 11115123

Cascales01: Cascales E, Lloubes R, Sturgis JN (2001). "The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB." Mol Microbiol 42(3);795-807. PMID: 11722743

Clavel98: Clavel T, Germon P, Vianney A, Portalier R, Lazzaroni JC (1998). "TolB protein of Escherichia coli K-12 interacts with the outer membrane peptidoglycan-associated proteins Pal, Lpp and OmpA." Mol Microbiol 29(1);359-67. PMID: 9701827

Click97: Click EM, Webster RE (1997). "Filamentous phage infection: required interactions with the TolA protein." J Bacteriol 179(20);6464-71. PMID: 9335297

Davies75: Davies JK, Reeves P (1975). "Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B." J Bacteriol 123(1);96-101. PMID: 124727

Derouiche95: Derouiche R, Benedetti H, Lazzaroni JC, Lazdunski C, Lloubes R (1995). "Protein complex within Escherichia coli inner membrane. TolA N-terminal domain interacts with TolQ and TolR proteins." J Biol Chem 270(19);11078-84. PMID: 7744737

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

FogniniLefebvre87: Fognini-Lefebvre N, Lazzaroni JC, Portalier R (1987). "tolA, tolB and excC, three cistrons involved in the control of pleiotropic release of periplasmic proteins by Escherichia coli K12." Mol Gen Genet 209(2);391-5. PMID: 3312962

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

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

Goemaere07: Goemaere EL, Devert A, Lloubes R, Cascales E (2007). "Movements of the TolR C-terminal domain depend on TolQR ionizable key residues and regulate activity of the Tol complex." J Biol Chem 282(24);17749-57. PMID: 17442676

Gully06: Gully D, Bouveret E (2006). "A protein network for phospholipid synthesis uncovered by a variant of the tandem affinity purification method in Escherichia coli." Proteomics 6(1);282-93. PMID: 16294310

Journet01: Journet L, Bouveret E, Rigal A, Lloubes R, Lazdunski C, Benedetti H (2001). "Import of colicins across the outer membrane of Escherichia coli involves multiple protein interactions in the periplasm." Mol Microbiol 42(2);331-44. PMID: 11703658

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

Kampfenkel93: Kampfenkel K, Braun V (1993). "Membrane topologies of the TolQ and TolR proteins of Escherichia coli: inactivation of TolQ by a missense mutation in the proposed first transmembrane segment." J Bacteriol 175(14);4485-91. PMID: 8331075

Karlsson03: Karlsson F, Borrebaeck CA, Nilsson N, Malmborg-Hager AC (2003). "The mechanism of bacterial infection by filamentous phages involves molecular interactions between TolA and phage protein 3 domains." J Bacteriol 185(8);2628-34. PMID: 12670988

Lazdunski98: Lazdunski CJ, Bouveret E, Rigal A, Journet L, Lloubes R, Benedetti H (1998). "Colicin import into Escherichia coli cells." J Bacteriol 180(19);4993-5002. PMID: 9748429

Lazzaroni02: Lazzaroni JC, Dubuisson JF, Vianney A (2002). "The Tol proteins of Escherichia coli and their involvement in the translocation of group A colicins." Biochimie 84(5-6);391-7. PMID: 12423782

Rigal97: Rigal A, Bouveret E, Lloubes R, Lazdunski C, Benedetti H (1997). "The TolB protein interacts with the porins of Escherichia coli." J Bacteriol 179(23);7274-9. PMID: 9393690

Sun86: Sun TP, Webster RE (1986). "fii, a bacterial locus required for filamentous phage infection and its relation to colicin-tolerant tolA and tolB." J Bacteriol 165(1);107-15. PMID: 3001021

UniProt10: UniProt Consortium (2010). "UniProt version 2010-07 released on 2010-06-15 00:00:00." Database.

UniProtGOA11: UniProt-GOA (2011). "Gene Ontology annotation based on the manual assignment of UniProtKB Subcellular Location terms in UniProtKB/Swiss-Prot entries."

UniProtGOA11a: UniProt-GOA (2011). "Gene Ontology annotation based on manual assignment of UniProtKB keywords in UniProtKB/Swiss-Prot entries."

Vianney96: Vianney A, Muller MM, Clavel T, Lazzaroni JC, Portalier R, Webster RE (1996). "Characterization of the tol-pal region of Escherichia coli K-12: translational control of tolR expression by TolQ and identification of a new open reading frame downstream of pal encoding a periplasmic protein." J Bacteriol 1996;178(14);4031-8. PMID: 8763928

Walburger02: Walburger A, Lazdunski C, Corda Y (2002). "The Tol/Pal system function requires an interaction between the C-terminal domain of TolA and the N-terminal domain of TolB." Mol Microbiol 44(3);695-708. PMID: 11994151

Zhang09: Zhang XY, Goemaere EL, Thome R, Gavioli M, Cascales E, Lloubes R (2009). "Mapping the Interactions between Escherichia coli Tol Subunits: ROTATION OF THE TolR TRANSMEMBRANE HELIX." J Biol Chem 284(7);4275-82. PMID: 19075020

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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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