Skip to main content

Advertisement

Log in

Expression and Regulation Pattern of Ferritin-like DpsA in the Archaeon Halobacterium Salinarum

  • Published:
Biometals Aims and scope Submit manuscript

Abstract

Very recently, an iron-rich protein, DpsA, was isolated from the extreme halophilic euryarchaeon Halobacterium salinarum JW5 and characterized. The amino acid sequence of DpsA is related to Dps proteins which belong structurally to the ferritin superfamily but differ from ferritins in their function and regulation. Employing Northern and Western blot analysis, the expression of DpsA in H. salinarum was examined throughout all growth phases and under a variety of growth conditions (iron deficiency, iron supplied growth, oxidative stress). DpsA shows increasing expression of dpsA mRNA in iron-rich media and under conditions of oxidative stress (H2O2), whereas under iron-deficient conditions mRNA-levels decrease. This is in contrast to Dps-type proteins the transcription of which is induced under conditions of iron starvation. Northern blot experiments show that the expression pattern of halobacterial DpsA is the same as that found in the few bacterial non-heme ferritin the expression pattern of which has been analyzed so far. Based on Western-blot analysis post-transcriptional regulation, typical of mammalian ferritins, can be excluded. This protein exhibits features of a non-heme type bacterial ferritin although it shares only little sequence similarity with Ftn from E. coli.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

Bfr:

DNA binding protein from starved cells

Dps:

heme containing bacterial ferritin

Ftn:

non-heme bacterial ferritin

References

  • H Abdul-Tehrani AJ Hudson Y-S Chang AR Timms C Hawkins JM Williams PM Harrison JR Guest SC Andrews (1999) ArticleTitleFerritin mutants of Escherichia coli are ion deficient and growth impaired, and fur mutants are iron deficient J Bacteriol 181 1415–1428 Occurrence Handle10049371

    PubMed  Google Scholar 

  • M Almirón AJ Link D Furlong R Kolter (1992) ArticleTitleA novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli Genes Dev 6 2646–2654 Occurrence Handle1340475

    PubMed  Google Scholar 

  • S Altuvia M Almirón G Huisman R Kolter G Storz (1994) ArticleTitleThe dps promoter is activated by OxyR during growth and by IHF and σS in stationary phase Mol Microbiol 13 265–272 Occurrence Handle7984106

    PubMed  Google Scholar 

  • SC. Andrews (1998) Iron Storage in Bacteria RK Poole (Eds) Adv Microb. Physiol NumberInSeriesvol. 40 Academic Press San Diego, London 281–351

    Google Scholar 

  • TA Azam S Hiraga A Ishihama (2000) ArticleTitleTwo types of localization of the DNA-binding proteins within the Escherichia coli nucleoid Genes Cells 5 613–626 Occurrence Handle10.1046/j.1365-2443.2000.00350.x Occurrence Handle10947847

    Article  PubMed  Google Scholar 

  • S Bereswill S Greiner AHM Van Vliet B Waidner F Fassbinder E Schlitz JG Kusters M Kist (2000) ArticleTitleRegulation of ferritin-mediated cytoplasmic iron storage by the ferric uptake regulator homolog (Fur) of Helicobacter pylori J Bacteriol 182 5948–5953 Occurrence Handle10.1128/JB.182.21.5948-5953.2000 Occurrence Handle11029412

    Article  PubMed  Google Scholar 

  • R Böhnke BF Matzanke (1995) ArticleTitleThe mobile ferrous iron pool in Escherichia coli is bound to a phosphorylated sugar derivative BioMetals 8 223–230 Occurrence Handle7647518

    PubMed  Google Scholar 

  • P Ceci A Ilari E Falvo E Chiancone (2003) ArticleTitleThe Dps protein of Agrobacterium tumefaciens does not bind to DNA, but protects it towards oxidative cleavage. X-ray crystal structure, iron binding and hydroxyl-radical scavenging properties J Biol Chem 278 20319–20326 Occurrence Handle10.1074/jbc.M302114200 Occurrence Handle12660233

    Article  PubMed  Google Scholar 

  • L Chen JD Helmann (1995) ArticleTitleBacillus subtilis MrgA is a Dps (PexB) homologue: Evidence for metalloregulation of an oxidative-stress gene Mol Microbiol 18 295–300 Occurrence Handle10.1111/j.1365-2958.1995.mmi_18020295.x Occurrence Handle8709848

    Article  PubMed  Google Scholar 

  • L Chen LP James JD Helmann (1993) ArticleTitleMetalloregulation in Bacillus subtilis: Isolation and characterization of two genes differentially repressed by metal ions J Bacteriol 175 5428–5437 Occurrence Handle8396117

    PubMed  Google Scholar 

  • H-J Choi S-J Kim P Mukhopadhyay S Cho J-R Woo G Storz S-E Ryo (2001) ArticleTitleStructural basis of the redox switch in the OxyR transcription factor Cell 105 103–113 Occurrence Handle10.1016/S0092-8674(01)00300-2 Occurrence Handle11301006

    Article  PubMed  Google Scholar 

  • P Chomczynski (1992) ArticleTitleOne-hour downward alkaline capillary transfer for blotting of DNA and RNA Anal Biochem 201 134–139 Occurrence Handle10.1016/0003-2697(92)90185-A Occurrence Handle1621951

    Article  PubMed  Google Scholar 

  • P Chomczynski N Sacchi (1987) ArticleTitleSingle-step method RNA isolation by acid guanidinium thiocyanate–phenol–chloroform Extraction Anal Biochem 162 156–159 Occurrence Handle2440339

    PubMed  Google Scholar 

  • I Delany ABF Pacheco G Spohn R Rappuoli V Scarlato (2001) ArticleTitleIron-dependent transcription of the frpB gene of Helicobacter pylori is controlled by the fur repressor protein J Bacteriol 183 4932–4937 Occurrence Handle10.1128/JB.183.16.4932-4937.2001 Occurrence Handle11466300

    Article  PubMed  Google Scholar 

  • L Escolar J Pérez-Martín V Lorenzo Particlede (1999) ArticleTitleOpening the iron box: Transcriptional metalloregulation by the fur protein J Bacteriol 181 6223–6229 Occurrence Handle10515908

    PubMed  Google Scholar 

  • DJ Evans SuffixJr. DG Evans T Takemura H Nakano HC Lampert DY Graham DN Granger PR Kvietys (1995) ArticleTitleCharacterization of a Helicobacter pylori neutrophil-activating protein Infect Immun 63 2213–2220 Occurrence Handle7768601

    PubMed  Google Scholar 

  • M Fuangthong AF Herbig N Bsat JD Helmann (2002) ArticleTitleRegulation of Bacillus subtilis fur and perR genes by PerR: Not all members of the PerR regulon are peroxide inducible J Bacteriol 184 3276–3286 Occurrence Handle10.1128/JB.184.12.3276-3286.2002 Occurrence Handle12029044

    Article  PubMed  Google Scholar 

  • RA Grant DJ Filman SE Finkel R Kolter JM Hogle (1998) ArticleTitleThe crystal structure of Dps, a ferritin homolog that binds and protects DNA Nature Struct Biol 5 294–303 Occurrence Handle10.1038/nsb0498-294 Occurrence Handle9546221

    Article  PubMed  Google Scholar 

  • S Gupta SB Pandit N Srinivasan D Chatterji (2002) ArticleTitleProteomics analysis of carbon-starved Mycobacterium smegmatis: induction of Dps-like protein Protein Eng 15 503–511 Occurrence Handle10.1093/protein/15.6.503 Occurrence Handle12082169

    Article  PubMed  Google Scholar 

  • K Hantke (2001) ArticleTitleIron and metal regulation in bacteria Curr Opin Microbiol 4 172–177 Occurrence Handle10.1016/S1369-5274(00)00184-3 Occurrence Handle11282473

    Article  PubMed  Google Scholar 

  • D Hubmacher BF Matzanke S Anemüller (2003) ArticleTitleEffects of iron limitation on the respiratory chain and the membrane cytochrome pattern of the Euryarchaeon Halobacterium salinarum Biol Chem 384 1565–1573 Occurrence Handle10.1515/BC.2003.173 Occurrence Handle14719798

    Article  PubMed  Google Scholar 

  • A Ilari S Stefanini E Chiancone D Tsernoglou (2000) ArticleTitleThe dodecameric ferritin from Listeria innocua contains a novel intersubunit iron-binding site Nature Struct Biol 7 38–43 Occurrence Handle10.1038/71236 Occurrence Handle10625425

    Article  PubMed  Google Scholar 

  • JA Imlay (2002) ArticleTitleHow oxygen damages microbes: Oxygen tolerance and obligate anaerobiosis Adv Microb Physiol 46 111–153 Occurrence Handlefull_text||10.1016/S0065-2911(02)46003-1 Occurrence Handle12073652

    Article  PubMed  Google Scholar 

  • T Ishikawa Y Mizunoe S-I Kawabata A Takade M Harada SN Wai S-I Yoshida (2003) ArticleTitleThe Iron-binding protein Dps confers hydrogen peroxide stress resistance to Campylobacter jejuni J Bacteriol 185 1010–1017 Occurrence Handle10.1128/JB.185.3.1010-1017.2003 Occurrence Handle12533477

    Article  PubMed  Google Scholar 

  • JK Lanyi (1974) ArticleTitleSalt-dependent properties of proteins from extremely halophilic bacteria Bacteriol Rev 38 272–290 Occurrence Handle4607500

    PubMed  Google Scholar 

  • I Listowsky G Blauer S Englard JJ Betheil (1972) ArticleTitleDenaturation of horse spleen ferritin in aqueous guanidinium chloride solutions Biochem 11 2176–2181 Occurrence Handle10.1021/bi00761a026

    Article  Google Scholar 

  • E Massé S Gottesman (2002) ArticleTitleA small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli Proc Natl Acad Sci USA 99 4620–4625 Occurrence Handle10.1073/pnas.032066599 Occurrence Handle11917098

    Article  PubMed  Google Scholar 

  • JP McHugh F Rodriguez-Quinones H Abdul-Tehrani DA Svistunenko RK Poole CE Cooper SC Andrews (2003) ArticleTitleGlobal iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis J Biol Chem 278 29478–29486 Occurrence Handle10.1074/jbc.M303381200 Occurrence Handle12746439

    Article  PubMed  Google Scholar 

  • S Mongkolsuk JD Helmann (2002) ArticleTitleRegulation of inducible peroxide stress response Mol Microbiol 45 9–15 Occurrence Handle10.1046/j.1365-2958.2002.03015.x Occurrence Handle12100544

    Article  PubMed  Google Scholar 

  • WV Ng SP Kennedy GG Mahairas B Berquist M Pan HD Shukla SR Lasky NS Baliga V Thorsson J Sbrogna S Swartzell D Weir J Hall TA Dahl R Welti YA Goo B Leithauser K Keller R Cruz MJ Danson DW Hough DG Maddocks PE Jablonski MP Krebs CM Angevine H Dale TA Isenbarger RF Peck M Pohlschroder JL Spudich KW Jung M Alam T Freitas S Hou CJ Daniels PP Dennis AD Omer H Ebhardt TM Lowe P Liang M Riley L Hood S DasSarma (2000) ArticleTitleGenome sequence of Halobacterium species NRC-1 Proc Natl Acad Sci USA 97 12176–12181 Occurrence Handle10.1073/pnas.190337797 Occurrence Handle11016950

    Article  PubMed  Google Scholar 

  • E Papinutto WG Dundon N Pitulis R Battistutta C Montecucco G Zanotti (2002) ArticleTitleStructure of two iron-binding proteins from Bacillus anthracis J Biol Chem 277 15093–15098 Occurrence Handle10.1074/jbc.M112378200 Occurrence Handle11836250

    Article  PubMed  Google Scholar 

  • MMO Pena GS Bullerjahn (1995a) ArticleTitleThe DpsA Protein of Synechococus sp. strain PCC 7942 is a DNA-binding hemoprotein J Biol Chem 270 22478–22482 Occurrence Handle10.1074/jbc.270.38.22478

    Article  Google Scholar 

  • MMO Pena W Burkhart GS Bullerjahn (1995) ArticleTitlePurification and characterization of a Synechococcus sp. strain PCC 7942 polypeptide structurally similar to the stress-induced Dps/PexB protein of Escherichia coli Arch Microbiol 163 337–344 Occurrence Handle7794101

    PubMed  Google Scholar 

  • M Polidoro D De Biase B Montagnini L Guarrera S Cavallo P Valenti S Stefanini E Chiancone (2002) ArticleTitleThe expression of the dodecameric ferritin in Listeria spp. is induced by iron limitation and stationary growth phase Gene 296 121–128 Occurrence Handle10.1016/S0378-1119(02)00839-9 Occurrence Handle12383509

    Article  PubMed  Google Scholar 

  • K Poster-Jordan EI Rosenberg JF Keiser JD Gross AM Ross S Nasim CT Garrett (1990) ArticleTitleNested polymerase chain reaction assay for the detection of cytomegalovirus overcomes false positives caused by contamination with fragmented DNA J Med Virol 30 85–91 Occurrence Handle2156009

    PubMed  Google Scholar 

  • AT Pulliainen S Haataja S Kähkönen J Finne (2003) ArticleTitleMolecular basis of H2O2 resistance mediated by Streptococcal Dps J Biol Chem 278 7996–8005 Occurrence Handle10.1074/jbc.M210174200 Occurrence Handle12501248

    Article  PubMed  Google Scholar 

  • Y Quian JH Lee RK Holmes (2002) ArticleTitleIdentification of a DtxR-regulated operon that is essential for siderophore-dependent iron uptake in Corynebacterium diphthiriae J Bacteriol 184 4846–4856 Occurrence Handle10.1128/JB.184.17.4846-4856.2002 Occurrence Handle12169610

    Article  PubMed  Google Scholar 

  • JN Reeve (2003) ArticleTitleArchaeal chromatin and transcription Mol Microbiol 48 587–598 Occurrence Handle10.1046/j.1365-2958.2003.03439.x Occurrence Handle12694606

    Article  PubMed  Google Scholar 

  • S Reindel S Anemüller A Sawaryn BF Matzanke (2002) ArticleTitleThe DpsA-homologue of the archaeon Halobacterium salinarum is a ferritin Biochim Biophys Acta 1598 140–146 Occurrence Handle12147354

    PubMed  Google Scholar 

  • B Ren G Tibbelin T Kajino O Asami R Ladenstein (2003) ArticleTitleThe multi-layered structuere of Dps with a novel di-nuclear ferroxidase center J Mol Biol 329 467–477 Occurrence Handle10.1016/S0022-2836(03)00466-2 Occurrence Handle12767829

    Article  PubMed  Google Scholar 

  • A Sen K Dwivedi KA Rice GS Bullerjahn (2000) ArticleTitleGrowth phase and metal-dependent regulation of the dpsA gene in Synechococcus sp. strain PCC 7942 Arch Microbiol 173 352–357 Occurrence Handle10.1007/s002030000153 Occurrence Handle10896214

    Article  PubMed  Google Scholar 

  • J. Soppa (2001) Basal and regulated transcription in Archaea P Blum (Eds) Adv Appl Microbiol NumberInSeriesvol. 50 Academic Press San Diego, New York, Boston, London, Sydney, Tokyo, Toronto 171–213

    Google Scholar 

  • K Sreeramulu CL Schmidt G Schäfer S Anemüller (1998) ArticleTitleStudies of the electron transport chain of the euryarcheon Halobacterium salinarum: Indications for a Type II NADH dehydrogenase and a complex III analog J Bioenerget Biomembr 30 443–453 Occurrence Handle10.1023/A:1020538129400

    Article  Google Scholar 

  • U Testa (2002) ArticleTitleRecent developments in the understaning of iron metabolism Hematol J 3 63–89 Occurrence Handle10.1038/sj.thj.6200163 Occurrence Handle12032869

    Article  PubMed  Google Scholar 

  • Tindall BJ (1992) The family halobacteriaceae. In The Prokaryotes, vol. second edition, Springer Verlag, pp. 768–808

  • F Tonello WG Dundon B Satin M Molinari G Tognon G Grandi G Del Giudice R Rappuoli C Montecucco (1999) ArticleTitleThe Helicobacter pylori neutrophil-activating protein is an iron-binding protein with dodecameric structure Mol Microbiol 34 238–246 Occurrence Handle10.1046/j.1365-2958.1999.01584.x Occurrence Handle10564468

    Article  PubMed  Google Scholar 

  • FM Torti SV Torti (2002) ArticleTitleRegulation of ferritin genes and protein Blood 99 3505–3516 Occurrence Handle10.1182/blood.V99.10.3505 Occurrence Handle11986201

    Article  PubMed  Google Scholar 

  • AHM Van Vliet J Stoof R Vlasblom SA Wainwright NJ Hughes DJ Kelly S Bereswill JJE Bijlsma T Hoogenboezem CMJE Vandenbroucke-Grauls M Kist EJ Kuipers JG Kusters (2002) ArticleTitleThe role of the ferric uptake regulater (Fur) in Regulation of Helicobacter pylori iron uptake Helicobacter 7 237–244 Occurrence Handle10.1046/j.1523-5378.2002.00088.x Occurrence Handle12165031

    Article  PubMed  Google Scholar 

  • B Waidner S Greiner S Odenbreit H Kavermann J Velayudhan F Stähler J Guhl E Bissé AHM Van Vliet SC Andrews JG Kusters DJ Kelly R Haas M Kist S Bereswill (2002) ArticleTitleEssential role of ferritin Pfr in Helicobacter pylori iron metabolism and gastric colonization Infect Immun 70 3923–3929 Occurrence Handle10.1128/IAI.70.7.3923-3929.2002 Occurrence Handle12065536

    Article  PubMed  Google Scholar 

  • Y Yamamoto M Higuchi LB Poole Y Kamio (2000) ArticleTitleRole of the dpr product in oxygen tolerance in Streptococcus mutans J Bacteriol 182 3740–3747 Occurrence Handle10.1128/JB.182.13.3740-3747.2000 Occurrence Handle10850989

    Article  PubMed  Google Scholar 

  • G Zanotti E Papinutto WG Dundon R Battistutta M Seveso G Del Giudice R Rappuoli C Montecucco (2002) ArticleTitleStructure of the neutrophil-activating protein from Helicobacter pylori J Mol Biol 323 125–130 Occurrence Handle10.1016/S0022-2836(02)00879-3 Occurrence Handle12368104

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Berthold F. Matzanke.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Reindel, S., Schmidt, C.L., Anemüller, S. et al. Expression and Regulation Pattern of Ferritin-like DpsA in the Archaeon Halobacterium Salinarum. Biometals 18, 387–397 (2005). https://doi.org/10.1007/s10534-005-3713-y

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-005-3713-y

Keywords

Navigation