Intracellular signal transfer in bacteria is dominated by phosphoryl transfer between conserved transmitter and receiver domains in regulatory proteins of so-called two-component systems. Escherichia coli contains 30 such systems, which allow it to modulate gene expression, enzyme activity and the direction of flagellar rotation. The authors have investigated whether, and to what extent, these separate systems form (an) interacting network(s) in vivo, focussing on interactions between four major systems, involved in the responses to the availability of phosphorylated sugars (Uhp), phosphate (Pho), nitrogen (Ntr) and oxygen (Arc). Significant cross-talk was not detectable in wild-type cells. Decreasing expression levels of succinate dehydrogenase (reporting Arc activation), upon activation of the Pho system, appeared to be independent of signalling through PhoR. Cross-talk towards NtrC did occur, however, in a ntrB deletion strain, upon joint activation of Pho, Ntr and Uhp. UhpT expression was demonstrated when cells were grown on pyruvate, through non-cognate phosphorylation of UhpA by acetyl phosphate.
AmemuraM., MakinoK., ShinagawaH.,
NakataA.1990; Cross talk to the phosphate regulon of Escherichia coli by PhoM protein: PhoM is a histidine protein kinase and catalyzes phosphorylation of PhoB and PhoM-open reading frame 2. J Bacteriol 172:6300–6307
ApplebyJ. L., ParkinsonJ. S.,
BourretR. B.1996; Signal transduction via the multi-step phosphorelay: not necessarily a road less traveled. Cell 86:845–848[CrossRef]
BackmanK. C., ChenY. M., Ueno-NishioS.,
MagasanikB.1983; The product of glnL is not essential for regulation of bacterial nitrogen assimilation. J Bacteriol 154:516–519
BeierD., SchwarzB., FuchsT. M.,
GrossR.1995; In vivo characterization of the unorthodox BvgS two-component sensor protein of Bordetella pertussis . J Mol Biol 248:596–610[CrossRef]
BouchéS., KlauckE., FischerD., LucassenM., JungK.,
Hengge-AronisR.1998; Regulation of RssB-dependent proteolysis in Escherichia coli : a role for acetyl phosphate in a response regulator-controlled process. Mol Microbiol 27:787–795[CrossRef]
BuenoR., PahelG.,
MagasanikB.1985; Role of glnB and glnD gene products in regulation of the glnALG operon of Escherichia coli . J Bacteriol 164:816–822
CotterP. A., ChepuriV., GennisR. B.,
GunsalusR. P.1990; Cytochrome o ( cyoABCDE ) and d ( cydAB )oxidase gene expression in Escherichia coli is regulated by oxygen, pH, and the fnr gene product. J Bacteriol 172:6333–6338
DaneseP. N., SnyderW. B., CosmaC. L., DavisL. J.,
SilhavyT. J.1995; The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9:387–398[CrossRef]
DorelC., VidalO., Prigent-CombaretC., ValletI.,
LejeuneP.1999; Involvement of the Cpx signal transduction pathway of E. coli in biofilm formation. FEMS Microbiol Lett 178:169–175[CrossRef]
FengJ., AtkinsonM. R., McClearyW., StockJ. B., WannerB. L.,
NinfaA. J.1992; Role of phosphorylated metabolic intermediates in the regulation of glutamine synthetase synthesis in Escherichia coli . J Bacteriol 174:6061–6070
FisherS. L., JiangW., WannerB. L.,
WalshC. T.1995; Cross-talk between the histidine protein kinase VanS and the response regulator PhoB. Characterization and identification of a VanS domain that inhibits activation of PhoB. J Biol Chem 270:23143–23149[CrossRef]
GeorgellisD., KwonO.,
LinE. C.1999; Amplification of signaling activity of the Arc two-component system of Escherichia coli by anaerobic metabolites. An in vitro study with different protein modules. J Biol Chem 274:35950–35954[CrossRef]
HellingwerfK. J., PostmaP. W., TommassenJ.,
WesterhoffH. V.1995; Signal transduction in bacteria: phospho-neural network(s) in Escherichia coli? FEMS. Microbiol Rev 16:309–321[CrossRef]
HellingwerfK. J., CrielaardW. C., HoffW. D., KortR., VerhammeD. T.,
Avignone-RossaC., Joost Teixeira de MattosM.1998; Current topics in signal transduction in bacteria. Antonie Leeuwenhoek 74:211–227[CrossRef]
HessJ. F., OosawaK., KaplanN.,
SimonM. I.1988; Phosphorylation of three proteins in the signaling pathway of bacterial chemotaxis. Cell 53:79–87[CrossRef]
HeydeM., LaloiP.,
PortalierR.2000; Involvement of carbon source and acetyl phosphate in the external-pH-dependent expression of porin genes in Escherichia coli . J Bacteriol 182:198–202[CrossRef]
IgoM. M., NinfaA. J.,
SilhavyT. J.1989; A bacterial environmental sensor that functions as a protein kinase and stimulates transcriptional activation. Genes Dev 3:598–605[CrossRef]
KadnerR. J.1995; Expression of the Uhp sugar-phosphate transport system of Escherichia coli . In Two-Component Signal Transduction pp 263–274 Edited by
HochJ. A.SilhavyT. J.
Washington, DC: American Society for Microbiology;
KimS. K., Wilmes-RiesenbergM. R.,
WannerB. L.1996; Involvement of the sensor kinase EnvZ in the in vivo activation of the response-regulator PhoB by acetyl phosphate. Mol Microbiol 22:135–147[CrossRef]
LynchA. S.,
LinE. C. C.others1996; Responses to molecular oxygen. In Escherichia coli and Salmonella: Cellular and Molecular Biology . , 2nd edn. pp 1526–1538 Edited by
NeidhardtF. C.
Washington, DC: American Society for Microbiology;
McClearyW. R.,
StockJ. B.1994; Acetyl phosphate and the activation of two-component response regulators. J Biol Chem 269:31567–31572
McFarlandN., McCarterL., ArtzS.,
KustuS.1981; Nitrogen regulatory locus glnR of enteric bacteria is composed of cistrons ntrB and ntrC : identification of their protein products. Proc Natl Acad Sci USA 78:2135–2139[CrossRef]
MagasanikB.1996; Regulation of nitrogen utilization. In Escherichia coli and Salmonella: Cellular and Molecular Biology . , 2nd edn. pp 1344–1356 Edited by
NeidhardtF. C.and others
Washington, DC: American Society for Microbiology;
MatsubaraM.,
MizunoT.1999; EnvZ-independent phosphotransfer signaling pathway of the OmpR-mediated osmoregulatory expression of OmpC and OmpF in Escherichia coli . Biosci Biotechnol Biochem 63:408–414[CrossRef]
MatsubaraM., KitaokaS. I., TakedaS. I.,
MizunoT.2000; Tuning of the porin expression under anaerobic growth conditions by His-to-Asp cross-phosphorelay through both the EnvZ-osmosensor and ArcB-anaerosensor in Escherichia coli . Genes Cells 5:555–569[CrossRef]
MatsushikaA.,
MizunoT.1998; A dual-signaling mechanism mediated by the ArcB hybrid sensor kinase containing the histidine-containing phosphotransfer domain in Escherichia coli . J Bacteriol 180:3973–3977
MichaelisS., InouyeH., OliverD.,
BeckwithJ.1983; Mutations that alter the signal sequence of alkaline phosphatase in Escherichia coli . J Bacteriol 154:366–374
MizunoT.1997; Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli . DNA Res 4:161–168[CrossRef]
NinfaA. J.,
MagasanikB.1986; Covalent modification of the glnG product, NRI, by the glnL product, NRII, regulates the transcription of the glnALG operon in Escherichia coli . Proc Natl Acad Sci USA 83:5909–5913[CrossRef]
NinfaA. J., NinfaE. G., LupasA. N., StockA., MagasanikB.,
StockJ.1988; Crosstalk between bacterial chemotaxis signal transduction proteins and regulators of transcription of the Ntr regulon: evidence that nitrogen assimilation and chemotaxis are controlled by a common phosphotransfer mechanism. Proc Natl Acad Sci USA 85:5492–5496[CrossRef]
ParkS. J., TsengC. P.,
GunsalusR. P.1995; Regulation of succinate dehydrogenase ( sdhCDAB ) operon expression in Escherichia coli in response to carbon supply and anaerobiosis: role of ArcA and Fnr. Mol Microbiol 15:473–482[CrossRef]
ParkS. J., ChaoG.,
GunsalusR. P.1997; Aerobic regulation of the sucABCD genes of Escherichia coli , which encode alpha-ketoglutarate dehydrogenase and succinyl coenzyme A synthetase: roles of ArcA, Fnr, and the upstream sdhCDAB promoter. J Bacteriol 179:4138–4142
PerraudA. L., KimmelB., WeissV.,
GrossR.1998; Specificity of the BvgAS and EvgAS phosphorelay is mediated by the C-terminal HPt domains of the sensor proteins. Mol Microbiol 27:875–887[CrossRef]
PrussB. M.1998; Acetyl phosphate and the phosphorylation of OmpR are involved in the regulation of the cell division rate in Escherichia coli . Arch Microbiol 170:141–146[CrossRef]
PrussB. M.,
WolfeA. J.1994; Regulation of acetyl phosphate synthesis and degradation, and the control of flagellar expression in Escherichia coli . Mol Microbiol 12:973–984[CrossRef]
RabinR. S.,
StewartV.1993; Dual response regulators (NarL and NarP) interact with dual sensors (NarX and NarQ) to control nitrate- and nitrite-regulated gene expression in Escherichia coli K-12. J Bacteriol 175:3259–3268
Shattuck-EidensD. M.,
KadnerR. J.1981; Exogenous induction of the Escherichia coli hexose phosphate transport system defined by uhp–lac operon fusions. J Bacteriol 148:203–209
SilvaJ. C., HaldimannA., PrahaladM. K., WalshC. T.,
WannerB. L.1998; In vivo characterization of the type A and B vancomycin-resistant enterococci (VRE) VanRS two-component systems in Escherichia coli : a nonpathogenic model for studying the VRE signal transduction pathways. Proc Natl Acad Sci USA 95:11951–11956[CrossRef]
SingerM., BakerT. A., SchnitzlerG.7 other authors1989; A collection of strains containing genetically linked alternating antibiotic resistance elements for genetic mapping of Escherichia coli . Microbiol Rev 53:1–24
WannerB. L.1995; Signal transduction and cross regulation in the Escherichia coli phosphate regulon by PhoR, CreC and acetyl phosphate. In Two-component Signal Transduction pp 203–221 Edited by
HochJ. A.SilhavyT. J.
Washington, DC: American Society for Microbiology;
WannerB. L.,
Wilmes-RiesenbergM. R.1992; Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli . J Bacteriol 174:2124–2130
WebberC. A.,
KadnerR. J.1995; Action of receiver and activator modules of UhpA in transcriptional control of the Escherichia coli sugar phosphate transport system. Mol Microbiol 15:883–893[CrossRef]
YakuH., KatoM., HakoshimaT., TsuzukiM.,
MizunoT.1997; Interaction between the CheY response regulator and the histidine-containing phosphotransfer (HPt) domain of the ArcB sensory kinase in Escherichia coli . FEBS Lett 408:337–340[CrossRef]
YamadaM., MakinoK., AmemuraM., ShinagawaH.,
NakataA.1989; Regulation of the phosphate regulon of Escherichia coli : analysis of mutant phoB and phoR genes causing different phenotypes. J Bacteriol 171:5601–5606