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Escherichia coli K-12 substr. MG1655 Polypeptide: starvation lipoprotein

Gene: slp Accession Numbers: EG11890 (EcoCyc), b3506, ECK3490

Regulation Summary Diagram: ?

Regulation summary diagram for slp

Slp (starvation lipoprotein) is the product of the slp gene [Alexander94a] which forms an operon with the downstream gene dctR [Tucker03]. Slp is believed to take part in acid resistance as expression increased when cells were grown at pH 5.5 and 4.5 under conditions known to induce glutamate-dependent acid resistance compared to pH 7.4 under the same conditions [Tucker02]. During growth in acidic conditions, expression of Slp is negatively regulated by GadW, but positively regulated by GadXW, which are regulators of the two glutamate decarboxylase genes and the GABA APC transporter responsible for glutamate-dependent acid resistance [Tucker03]. slp is highly induced by overexpression of EvgA [Masuda02], [Nishino03] indirectly through its induction of YdeO expression [Ma04], though slp was found to have a putative EvgA binding motif 542 base pairs upstream of its start codon [Nishino03].

Under certain conditions, deletion of slp-dctR resulted in reduction of YdeO-induced acid resistance [Masuda03], though under conditions used to induce acid resistance naturally, slp-dctR was not necessary [Ma04]. A slp-dctR double mutant exhibited loss of viability during growth in spent LB at pH 2.5 much faster than wild-type [Mates07]. The slp-dctR double mutant was also unable to survive at pH 2.5 in minimal medium when formate, succinate, or lactate were added [Mates07]. The fact that individual slp and dctR mutants retain resistance indicates redundant functions for Slp and DctR in protection against formate, succinate, and lactate at low pH [Mates07].

slp is upregulated when cells are deprived of carbon or during stationary phase [Alexander94a]. Expression of slp increases 3-5 fold in stationary phase [Shimada04]. This has been shown under certain conditions to occur independently of RpoS, cAMP, and DnaK [Alexander94a], while under other conditions the promoter for slp is RpoS sigma-dependent [Shimada04]. Expression of slp is reduced after 10 hours of nitrogen starvation in an rpoS mutant [Kabir04a]. Sequence analysis suggests slp may also be controlled by a sigma 70 promoter [Alexander94a].

Slp expression is reduced by constitutive expression of marRAB, which is responsible for multiple antibiotic resistance [Seoane95a]. The Mar system affects Slp expression during the transition from exponential to stationary phase, though not the final stationary phase level. Cells show some increased chloramphenicol sensitivity when Slp levels increase [Price00].

The level of Slp expression increased in response to exposure to acetate [Arnold01] and acivicin [Smulski01], in the presence of the transcriptional regulator SlyA in the enteroinvasive E. coli strain 12860 [Spory02], when the leucine-responsive regulatory protein is not expressed [Tani02], and upon deletion of hns, encoding the H-NS transcriptional duel regulator [Nishino04]. Slp is strongly induced under anaerobic growth, but repression occurs after addition of nitrate [Brokx04]. Other factors that reduce Slp expression include filamentous phage infection [Karlsson05], adhesion of cells to abiotic surfaces [Otto01], and the expression of SulA, though this is suggested to be more likely the result of a response to physiological alterations due to blockage of cell division [Arends04].

Slp was found as higher order oligomers tethered to the outer membrane [Stenberg05].

Locations: outer membrane

Map Position: [3,651,984 -> 3,652,550] (78.71 centisomes, 283°)
Length: 567 bp / 188 aa

Molecular Weight of Polypeptide: 20.964 kD (from nucleotide sequence), 22 kD (experimental) [Alexander94a ]

Unification Links: ASAP:ABE-0011451 , CGSC:33726 , EchoBASE:EB1836 , EcoGene:EG11890 , EcoliWiki:b3506 , OU-Microarray:b3506 , PortEco:slp , PR:PRO_000023955 , Pride:P37194 , Protein Model Portal:P37194 , RefSeq:NP_417963 , RegulonDB:EG11890 , String:511145.b3506 , UniProt:P37194

Relationship Links: InterPro:IN-FAMILY:IPR004658 , Pfam:IN-FAMILY:PF03843 , Prosite:IN-FAMILY:PS51257

In Paralogous Gene Group: 534 (2 members)

Genetic Regulation Schematic: ?

Genetic regulation schematic for slp

GO Terms:

Molecular Function: GO:0042802 - identical protein binding Inferred from experiment [Rajagopala14, Stenberg05]
Cellular Component: GO:0019867 - outer membrane Inferred from experiment Inferred by computational analysis [GOA01a, Stenberg05]
GO:0009279 - cell outer membrane Inferred by computational analysis [UniProtGOA11, UniProtGOA11a, Alexander94a]
GO:0016020 - membrane Inferred by computational analysis [UniProtGOA11a]

MultiFun Terms: cell processes adaptations starvation

Essentiality data for slp knockouts: ?

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

Last-Curated ? 16-Apr-2007 by Johnson A , TIGR

Sequence Features

Protein sequence of starvation lipoprotein with features indicated

Feature Class Location Citations Comment
Signal-Sequence 1 -> 18
Lipid-Binding-Site 19
[Alexander94a, UniProt15]
UniProt: N-palmitoyl cysteine.
Chain 19 -> 188
UniProt: Outer membrane protein slp;

Gene Local Context (not to scale): ?

Gene local context diagram

Transcription Unit:

Transcription-unit diagram


Martin Peralta on Fri Oct 29, 2004:
The start site of this gene was originally assigned solely on the basis of sequence considerations (Blattner et al, 1997, [Blattner97 ]. However, it was changed because Alexander et al (1994) attested that the real start site is actually located in another position [Alexander94a ]. The demonstration is based on (a) comparisons of the new gene sequence with homologous proteins, (b) determination of the mRNA size (Northern blot), plus (c) identification of both a plausible ribosome binding site and a promoter at an appropriate distance from the new start site. The promoter was identified using primer extension analysis.
1/26/1998 (pkarp) Merged genes G7973/slp and EG11890/slp


Alexander94a: Alexander DM, St John AC (1994). "Characterization of the carbon starvation-inducible and stationary phase-inducible gene slp encoding an outer membrane lipoprotein in Escherichia coli." Mol Microbiol 1994;11(6);1059-71. PMID: 8022277

Arends04: Arends SJ, Weiss DS (2004). "Inhibiting cell division in Escherichia coli has little if any effect on gene expression." J Bacteriol 186(3);880-4. PMID: 14729718

Arnold01: Arnold CN, McElhanon J, Lee A, Leonhart R, Siegele DA (2001). "Global analysis of Escherichia coli gene expression during the acetate-induced acid tolerance response." J Bacteriol 183(7);2178-86. PMID: 11244055

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

Blattner97: Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997). "The complete genome sequence of Escherichia coli K-12." Science 277(5331);1453-74. PMID: 9278503

Brokx04: Brokx SJ, Ellison M, Locke T, Bottorff D, Frost L, Weiner JH (2004). "Genome-wide analysis of lipoprotein expression in Escherichia coli MG1655." J Bacteriol 186(10);3254-8. PMID: 15126489

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

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

Kabir04a: Kabir MS, Sagara T, Oshima T, Kawagoe Y, Mori H, Tsunedomi R, Yamada M (2004). "Effects of mutations in the rpoS gene on cell viability and global gene expression under nitrogen starvation in Escherichia coli." Microbiology 150(Pt 8);2543-53. PMID: 15289551

Karlsson05: Karlsson F, Malmborg-Hager AC, Albrekt AS, Borrebaeck CA (2005). "Genome-wide comparison of phage M13-infected vs. uninfected Escherichia coli." Can J Microbiol 51(1);29-35. PMID: 15782232

Ma04: Ma Z, Masuda N, Foster JW (2004). "Characterization of EvgAS-YdeO-GadE branched regulatory circuit governing glutamate-dependent acid resistance in Escherichia coli." J Bacteriol 186(21);7378-89. PMID: 15489450

Masuda02: Masuda N, Church GM (2002). "Escherichia coli gene expression responsive to levels of the response regulator EvgA." J Bacteriol 184(22);6225-34. PMID: 12399493

Masuda03: Masuda N, Church GM (2003). "Regulatory network of acid resistance genes in Escherichia coli." Mol Microbiol 48(3);699-712. PMID: 12694615

Mates07: Mates AK, Sayad AK, Foster JW (2007). "Products of the Escherichia coli Acid Fitness Island Attenuate Metabolite Stress at Extreme Low pH and Mediate a Cell Density-Dependent Acid Resistance." J Bacteriol 189(7):2759-68. PMID: 17259322

Nishino03: Nishino K, Inazumi Y, Yamaguchi A (2003). "Global analysis of genes regulated by EvgA of the two-component regulatory system in Escherichia coli." J Bacteriol 185(8);2667-72. PMID: 12670992

Nishino04: Nishino K, Yamaguchi A (2004). "Role of histone-like protein H-NS in multidrug resistance of Escherichia coli." J Bacteriol 186(5);1423-9. PMID: 14973023

Otto01: Otto K, Norbeck J, Larsson T, Karlsson KA, Hermansson M (2001). "Adhesion of type 1-fimbriated Escherichia coli to abiotic surfaces leads to altered composition of outer membrane proteins." J Bacteriol 183(8);2445-53. PMID: 11274103

Price00: Price GP, St John AC (2000). "Purification and analysis of expression of the stationary phase-inducible slp lipoprotein in Escherichia coli: role of the Mar system." FEMS Microbiol Lett 193(1);51-6. PMID: 11094278

Rajagopala14: Rajagopala SV, Sikorski P, Kumar A, Mosca R, Vlasblom J, Arnold R, Franca-Koh J, Pakala SB, Phanse S, Ceol A, Hauser R, Siszler G, Wuchty S, Emili A, Babu M, Aloy P, Pieper R, Uetz P (2014). "The binary protein-protein interaction landscape of Escherichia coli." Nat Biotechnol 32(3);285-90. PMID: 24561554

Seoane95a: Seoane AS, Levy SB (1995). "Identification of new genes regulated by the marRAB operon in Escherichia coli." J Bacteriol 177(3);530-5. PMID: 7836283

Shimada04: Shimada T, Makinoshima H, Ogawa Y, Miki T, Maeda M, Ishihama A (2004). "Classification and strength measurement of stationary-phase promoters by use of a newly developed promoter cloning vector." J Bacteriol 186(21);7112-22. PMID: 15489422

Smulski01: Smulski DR, Huang LL, McCluskey MP, Reeve MJ, Vollmer AC, Van Dyk TK, LaRossa RA (2001). "Combined, functional genomic-biochemical approach to intermediary metabolism: interaction of acivicin, a glutamine amidotransferase inhibitor, with Escherichia coli K-12." J Bacteriol 183(11);3353-64. PMID: 11344143

Spory02: Spory A, Bosserhoff A, von Rhein C, Goebel W, Ludwig A (2002). "Differential regulation of multiple proteins of Escherichia coli and Salmonella enterica serovar Typhimurium by the transcriptional regulator SlyA." J Bacteriol 2002;184(13);3549-59. PMID: 12057949

Stenberg05: Stenberg F, Chovanec P, Maslen SL, Robinson CV, Ilag LL, von Heijne G, Daley DO (2005). "Protein complexes of the Escherichia coli cell envelope." J Biol Chem 280(41);34409-19. PMID: 16079137

Tani02: Tani TH, Khodursky A, Blumenthal RM, Brown PO, Matthews RG (2002). "Adaptation to famine: a family of stationary-phase genes revealed by microarray analysis." Proc Natl Acad Sci U S A 99(21);13471-6. PMID: 12374860

Tucker02: Tucker DL, Tucker N, Conway T (2002). "Gene expression profiling of the pH response in Escherichia coli." J Bacteriol 184(23);6551-8. PMID: 12426343

Tucker03: Tucker DL, Tucker N, Ma Z, Foster JW, Miranda RL, Cohen PS, Conway T (2003). "Genes of the GadX-GadW regulon in Escherichia coli." J Bacteriol 185(10);3190-201. PMID: 12730179

UniProt09: UniProt Consortium (2009). "UniProt version 15.8 released on 2009-10-01 00:00:00." Database.

UniProt15: UniProt Consortium (2015). "UniProt version 2015-01 released on 2015-01-16 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."

Other References Related to Gene Regulation

Hirakawa10: Hirakawa H, Hayashi-Nishino M, Yamaguchi A, Nishino K (2010). "Indole enhances acid resistance in Escherichia coli." Microb Pathog 49(3);90-4. PMID: 20470880

Johnson11: Johnson MD, Burton NA, Gutierrez B, Painter K, Lund PA (2011). "RcsB Is Required for Inducible Acid Resistance in Escherichia coli and Acts at gadE-Dependent and -Independent Promoters." J Bacteriol 193(14);3653-6. PMID: 21571995

Krin10: Krin E, Danchin A, Soutourina O (2010). "Decrypting the H-NS-dependent regulatory cascade of acid stress resistance in Escherichia coli." BMC Microbiol 10;273. PMID: 21034467

Krin10a: Krin E, Danchin A, Soutourina O (2010). "RcsB plays a central role in H-NS-dependent regulation of motility and acid stress resistance in Escherichia coli." Res Microbiol 161(5);363-371. PMID: 20435136

Tramonti08: Tramonti A, De Canio M, De Biase D (2008). "GadX/GadW-dependent regulation of the Escherichia coli acid fitness island: transcriptional control at the gadY-gadW divergent promoters and identification of four novel 42 bp GadX/GadW-specific binding sites." Mol Microbiol 70(4);965-82. PMID: 18808381

Yamanaka14: Yamanaka Y, Oshima T, Ishihama A, Yamamoto K (2014). "Characterization of the YdeO regulon in Escherichia coli." PLoS One 9(11);e111962. PMID: 25375160

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