Skip to main content
SpringerLink
Log in

The three-component signalling system HbpS–SenS–SenR as an example of a redox sensing pathway in bacteria

  • Review Article
  • Published:
Amino Acids Aims and scope Submit manuscript

Abstract

The two-component system SenS–SenR and the extracellular HbpS protein of the cellulose degrader Streptomyces reticuli have been shown to act in concert as a novel system which detects redox stress. In vivo and in vitro experiments have led to the hypothesis that HbpS binds and degrades heme, communicating the extracellular presence of heme and oxidative stress to the membrane-embedded sensor histidine kinase SenS via a bound iron. The response regulator SenR would then up-regulate downstream signalling cascades, leading to the appropriate gene expression levels for bacterial survival in an oxidative environment. Sequence analysis has shown that homologs of HbpS and SenS–SenR exist in a number of ecologically and medically relevant bacterial species, suggesting the existence of a previously undescribed bacterial oxidative stress-response pathway common to both Gram-negative and Gram-positive bacteria. The presented report reviews the current knowledge of the function of this novel protein family consisting of an accessory protein and its cognate two-component system, which could be more properly described as a three-component system.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alm E, Huang K, Arkin A (2006) The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLoS Comput Biol 2:e143

    Article  PubMed  Google Scholar 

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipmann DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Baker HM, Anderson BF, Baker EN (2003) Dealing with iron: common structural principles in proteins that transport iron and heme. Proc Natl Acad Sci USA 100:3579–3583

    Article  PubMed  CAS  Google Scholar 

  • Baldrian P, Valášková V (2008) Degradation of cellulose by basidiomycetous fungi. FEMS Microbiol Rev 32:501–521

    Article  PubMed  CAS  Google Scholar 

  • Baltz RH (2006) Molecular engineering approaches to peptide, polyketide and other antibiotics. Nat Biotechnol 24:1533–1540

    Article  PubMed  CAS  Google Scholar 

  • Berks BC, Sargent F, Palmer T (2000) The Tat protein export pathway. Mol Microbiol 35:260–274

    Article  PubMed  CAS  Google Scholar 

  • Bogel G, Schrempf H, Ortiz de Orué Lucana D (2007) DNA-binding characteristics of the regulator SenR in response to phosphorylation by the sensor histidine autokinase SenS from Streptomyces reticuli. FEBS J 274:3900–3913

    Article  PubMed  CAS  Google Scholar 

  • Bogel G, Schrempf H, Ortiz de Orué Lucana D (2008) The heme-binding protein HbpS regulates the activity of the Streptomyces reticuli iron-sensing histidine kinase SenS in a redox-dependent manner. Amino Acids. doi:10.1007/s00726-008-0188-5

  • Cash TP, Pan Y, Simon MC (2007) Reactive oxygen species and cellular oxygen sensing. Free Radic Biol Med 43:1219–1225

    Article  PubMed  CAS  Google Scholar 

  • Challis GL, Hopwood DA (2003) Synergy and contingency as driving forces for the evolution of multiple secondary metabolite production by Streptomyces species. Proc Natl Acad Sci USA 100:14555–145561

    Article  PubMed  CAS  Google Scholar 

  • Claus H, Decker H (2006) Bacterial tyrosinases. Syst Appl Microbiol 29:3–14

    Article  PubMed  CAS  Google Scholar 

  • Crosson S, McGrath PT, Stephens C, McAdams HH, Shapiro L (2005) Conserved modular design of an oxygen sensory/signalling network with species-specific output. Proc Natl Acad Sci USA 102:8018–8023

    Article  PubMed  CAS  Google Scholar 

  • Deng DM, Liu MJ, ten Cate JM, Crielaard W (2007) The VicRK system of Streptococcus mutans responds to oxidative stress. J Dent Res 86:606–610

    Article  PubMed  CAS  Google Scholar 

  • DiGiuseppe PA, Silhavy TJ (2003) Signal detection and target gene induction by the CpxRA two-component system. J Bacteriol 185:2432–2440

    Article  PubMed  CAS  Google Scholar 

  • Elsen S, Dúche O, Colbeau A (2003) Interaction between the sensor HupUV and the histidine kinase HupT controls HupSL hydrogenase synthesis in Rhodobacter capsulatus. J Bacteriol 185:7111–7119

    Article  PubMed  CAS  Google Scholar 

  • Fabret C, Feher VA, Hoch JA (1999) Two-component signal transduction in Bacillus subtilis: how one organism sees its world. J Bacteriol 181:1975–1983

    PubMed  CAS  Google Scholar 

  • Fenton HJH (1986) Oxidation of tartaric acid in the presence of iron. J Chem Soc 65:899–910

    Google Scholar 

  • Flardh K (2003) Growth polarity and cell division in Streptomyces. Curr Opin Microbiol 6:564–571

    Article  PubMed  CAS  Google Scholar 

  • Garnerone AM, Cabanes D, Foussard M, Boistard P, Batut J (1999) Inhibition of the FixL sensorkinase by the FixT protein in Sinorhizobium meliloti. J Biol Chem 274:32500–32506

    Article  PubMed  CAS  Google Scholar 

  • Hantke K (2001) Iron and metal regulation in bacteria. Curr Opin Microbiol 4:172–177

    Article  PubMed  CAS  Google Scholar 

  • Hoch JA, Varughese KI (2001) Keeping signals straight in phosphorelay signal transduction. J Bacteriol 183:4941–4949

    Article  PubMed  CAS  Google Scholar 

  • Hoskisson PA, Hutchings MI (2006) MtrAB-LpqB: a conserved three-component system in actinobacteria? Trends Microbiol 14:444–449

    Article  PubMed  CAS  Google Scholar 

  • Hutchings MI, Hoskisson PA, Chandra G, Buttner MJ (2004) Sensing and responding to diverse extracellular signals? Analysis of the sensor kinases and response regulators of Streptomyces coelicolor A3(2). Microbiology 150:2795–2806

    Article  PubMed  CAS  Google Scholar 

  • Hutchings MI, Hong HJ, Leibovitz E, Sutcliffe IC, Buttner MJ (2006) The sigma(E) cell envelope stress response of Streptomyces coelicolor is influenced by a novel lipoprotein, CseA. J Bacteriol 188:7222–7229

    Article  PubMed  CAS  Google Scholar 

  • Ioanoviciu A, Yukl ET, Moёnne-Loccoz P, de Montellano PR (2007) DevS, a heme-containing two-component sensor of Mycobacterium tuberculosis. Biochemistry 46:4250–4260

    Article  PubMed  CAS  Google Scholar 

  • Jubelin G, Vianney A, Beloin C, Ghigo JM, Lazzaroni JC, Lejeune P, Dorel C (2005) CpxR/OmpR interplay regulates curli gene expression in response to osmolarity in Escherichia coli. J Bacteriol 187:2038–2049

    Article  PubMed  CAS  Google Scholar 

  • Klein BS, Tebbets (2007) Dimorphism and virulence in fungi. Curr Opin Microbiol 10:314–319

  • Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ (2007) A common mechanism of cellular death induced by bactericidal antibiotics. Cell 130:797–810

    Article  PubMed  CAS  Google Scholar 

  • Kohanski MA, Dwyer DJ, Wierzbowski J, Cottarel G, Collins JJ (2008) Mistranslation of membrane proteins and two-component system activation trigger antibiotic-mediated cell death. Cell 135:679–690

    Article  PubMed  CAS  Google Scholar 

  • Kumar A, Toledo JC, Patel RP, Lancaster JR, Steyn AJ Jr (2007) Mycobacterium tuberculosis DosS is a redox sensor and DosT is a hypoxia sensor. Proc Natl Acad Sci USA 104:11568–11573

    Article  PubMed  CAS  Google Scholar 

  • Laub MT, Goulian M (2007) Specificity in two component signal transduction pathways. Annu Rev Genet 41:121–145

    Article  PubMed  CAS  Google Scholar 

  • Lee AI, Delgado A, Gunsalus RP (1999) Signal-dependent phosphorylation of the membrane-bound NarX two-component sensor-transmitter protein of Escherichia coli: nitrate elicits a superior anion ligand response compared to nitrite. J Bacteriol 181:5309–5316

    PubMed  CAS  Google Scholar 

  • Lindemann A, Moser A, Pessi G, Hauser F, Friberg M, Hennecke H, Fischer HM (2007) New target genes controlled by the Bradyrhizobium japonicum two-component regulatory system RegSR. J Bacteriol 189:8928–8943

    Article  PubMed  CAS  Google Scholar 

  • Malpica R, Franco B, Rodriguez C, Kwon O, Georgellis D (2004) Identification of a quinone-sensitive redox switch in the ArcB sensor kinase. Proc Natl Acad Sci USA 101:13318–13323

    Article  PubMed  CAS  Google Scholar 

  • Mascher T, Helmann JD, Unden G (2006) Stimulus perception in bacterial signal-transducing histidine kinases. Microbiol Mol Biol Rev 70:910–938

    Article  PubMed  CAS  Google Scholar 

  • Mizuno T (1997) Compilation of all genes encoding two-component phosphotransfer signal transducers in the genome of Escherichia coli. DNA Res 4:161–168

    Article  PubMed  CAS  Google Scholar 

  • Nagababu E, Rifkind JM (2004) Heme degradation by reactive oxygen species. Antioxid Redox Signal 6:967–978

    PubMed  CAS  Google Scholar 

  • Nemecek JC, Wüthrich M, Klein BS (2006) Global control of dimorphism and virulence in fungi. Science 28:583–588

    Article  Google Scholar 

  • Nishino K, Hsu FF, Turk J, Cromie MJ, Wösten MMSM, Groisman EA (2006) Identification of the lipopolysaccharide modifications controlled by the Salmonella PmrA/PmrB system mediating resistance to Fe(III) and Al(III). Mol Microbiol 61:645–654

    Article  PubMed  CAS  Google Scholar 

  • Novick RP, Geisinger E (2008) Quorum sensing in staphylococci. Annu Rev Genet 42:541–564

    Article  PubMed  CAS  Google Scholar 

  • Ortiz de Orué Lucana D, Troller M, Schrempf H (2003) Amino acid residues involved in reversible thiol formation and zinc ion binding in the Streptomyces reticuli redox regulator FurS. Mol Genet Genomics 268:618–627

    PubMed  Google Scholar 

  • Ortiz de Orué Lucana D, Schaa T, Schrempf H (2004) The novel extracellular Streptomyces reticuli haem-binding protein HbpS influences the production of the catalase-peroxidase CpeB. Microbiology 150:2575–2585

    Article  PubMed  Google Scholar 

  • Ortiz de Orué Lucana D, Zou P, Nierhaus M, Schrempf H (2005) Identification of a novel two-component system SenS/SenR modulating the production of the catalase-peroxidase CpeB and the haem-binding protein HbpS in Streptomyces reticuli. Microbiology 151:3603–3614

    Article  PubMed  Google Scholar 

  • Ortiz de Orué Lucana D, Bogel G, Zou P, Groves MR (2009) The oligomeric assembly of the novel haem degrading protein HbpS is essential for interaction with its cognate two-component sensor kinase. J Mol Biol 386:1108–1122

    Article  PubMed  Google Scholar 

  • Panek H, O’Brian MR (2002) A whole genome view of prokaryotic haem biosynthesis. Microbiology 148:2273–2282

    PubMed  CAS  Google Scholar 

  • Polizeli ML, Rizzatti AC, Monti R, Terenzi HF, Jorge JA, Amorim DS (2005) Xylanases from fungi: properties and industrial applications. Appl Microbiol Biotechnol 67:577–591

    Article  PubMed  CAS  Google Scholar 

  • Rietkötter E, Hoyer D, Mascher T (2008) Bacitracin sensing in Bacillus subtilis. Mol Microbiol 68:768–785

    Article  PubMed  Google Scholar 

  • Rietsch A, Beckwith J (1998) The genetics of disulfide bond metabolism. Annu Rev Genet 32:163–184

    Article  PubMed  CAS  Google Scholar 

  • Rudolph G, Hennecke H, Fischer HM (2006) Beyond the Fur paradigm: iron-controlled gene expression in rhizobia. FEMS Microbiol Rev 30:631–648

    Article  PubMed  CAS  Google Scholar 

  • Sala C, Forti E, Di Florio F, Canneva F, Milano A, Riccardi G, Ghisotti D (2003) Mycobacterium tuberculosis FurA autoregulates its own expression. J Bacteriol 185:5357–5362

    Article  PubMed  CAS  Google Scholar 

  • Schaerlaekens K, Schierova M, Lammertyn E, Geukens N, Anné J, van Mellaert L (2001) Twin-arginine translocation pathway in Streptomyces lividans. J Bacteriol 183:6727–6732

    Article  PubMed  CAS  Google Scholar 

  • Schlochtermeier A, Walter S, Schröder J, Moormann M, Schrempf H (1992) The gene encoding the cellulase (Avicelase) Cel1 from Streptomyces reticuli and analysis of protein domains. Mol Microbiol 6:3611–3621

    Article  PubMed  CAS  Google Scholar 

  • Schmitt MP (1999) Identification of a two-component signal transduction system from Corynebacterium diphteriae that activates gene expression in response to the presence of heme and hemoglobin. J Bacteriol 181:5330–5340

    PubMed  CAS  Google Scholar 

  • Sherman DR, Mdluli K, Hickey MJ, Arain TM, Morris SL, Barry CE III, Stover CK (1996) Compensatory ahpC gene expression in isoniazid-resistant Mycobacterium tuberculosis. Science 272:1641–1643

    Article  PubMed  CAS  Google Scholar 

  • Sonnhammer ELL, Eddy SR, Durbin R (1997) Pfam: a comprehensive database of protein families based on seed alignments. Proteins 28:405–420

    Article  PubMed  CAS  Google Scholar 

  • Stauff DL, Torres VJ, Skaar EP (2007) Signaling and DNA-binding activities of the Staphylococcus aureus HssR–HssS two-component system required for heme sensing. J Biol Chem 282(36):26111–26121

    Article  PubMed  CAS  Google Scholar 

  • Szurmant H, Nelson K, Kim EJ, Perego M, Hoch JA (2005) YycH regulates the activity of the essential YycFG two-component system in Bacillus subtilis. J Bacteriol 187:5419–5426

    Article  PubMed  CAS  Google Scholar 

  • Szurmant H, Bu L, Brooks CLIII, Hoch JA (2008) An essential sensor histidine kinase controlled by transmembrane helix interactions with its auxiliary proteins. Proc Natl Acad Sci USA 105:5891–5896

    Article  PubMed  CAS  Google Scholar 

  • Timmen M, Bassler BL, Jung K (2006) AI-1 influences the kinase activity but not the phosphatase activity of LuxN of Vibrio harveyi. J Biol Chem 281:24398–24404

    Article  PubMed  CAS  Google Scholar 

  • To JP, Kieber JJ (2008) Cytokinin signaling: two-components and more. Trends Plant Sci 13:85–92

    Article  PubMed  CAS  Google Scholar 

  • Wei W, Wang W, Cao Z, Yu H, Wang X, Zhao J, Tan H, Xu H, Jiang W, Li Y (2007) Comparative analysis of two-component signal transduction system in two streptomycete genomes Acta Biochim Biophys Sin (Shanghai) 39:317–325

    Google Scholar 

  • Wösten MM, Kox LF, Chamnongpol S, Soncini FC, Groisman EA (2000) A signal transduction system that responds to extracellular iron. Cell 103:113–125

    Article  PubMed  Google Scholar 

  • Yoshida T, Cai S, Inouye M (2002) Interaction of EnvZ, a sensory histidine kinase, with phosphorylated OmpR, the cognate response regulator. Mol Microbiol 46:1283–1294

    Article  PubMed  CAS  Google Scholar 

  • Zapf J, Sen U, Madhusudan HochJA, Varughese KI (2000) A transient interaction between two phosphorelay proteins trapped in a crystal lattice reveals the mechanism of molecular recognition and phosphotransfer in signal transduction. Structure 15:851–862

    Article  Google Scholar 

  • Zou P, Schrempf H (2000) The heme-independent manganese-peroxidase activity depends on the presence of the C-terminal domain within the Streptomyces reticuli catalase-peroxidase CpeB. Eur J Biochem 267:2840–2849

    Article  PubMed  CAS  Google Scholar 

  • Zou P, Groves MR, Viale-Bouroncle SD, Ortiz de Orué Lucana D (2008) Crystallization and preliminary characterization of a novel haem-binding protein of Streptomyces reticuli. Acta Crystallogr Sect F Struct Biol Cryst Commun 64:386–390

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We are very grateful to all our collaborators in particular to Prof. Dr. H. Schrempf, Dr. G. Bogel and Dr. P. Zou.

Author information

Authors and Affiliations

  1. FB Biologie/Chemie, Angewandte Genetik der Mikroorganismen, Universität Osnabrück, Barbarastr. 13, 49069, Osnabrück, Germany

    Darío Ortiz de Orué Lucana

  2. EMBL Hamburg Outstation, c/o DESY, Building 25A, Notkestrasse 85, 22603, Hamburg, Germany

    Matthew R. Groves

Authors
  1. Darío Ortiz de Orué Lucana
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Matthew R. Groves
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Darío Ortiz de Orué Lucana.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ortiz de Orué Lucana, D., Groves, M.R. The three-component signalling system HbpS–SenS–SenR as an example of a redox sensing pathway in bacteria. Amino Acids 37, 479–486 (2009). https://doi.org/10.1007/s00726-009-0260-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-009-0260-9

Keywords

Search

Navigation