Skip to main content
SpringerLink
Log in

The bacterial metallome: composition and stability with specific reference to the anaerobic bacterium Desulfovibrio desulfuricans

  • Published:
BioMetals Aims and scope Submit manuscript

Abstract

In bacteria, the intracellular metal content or metallome reflects the metabolic requirements of the cell. When comparing the composition of metals in phytoplankton and bacteria that make up the macronutrients and the trace elements, we have determined that the content of trace elements in both of these microorganisms is markedly similar. The trace metals consisting of transition metals plus zinc are present in a stoichometric molar formula that we have calculated to be as follows: Fe1Mn0.3Zn0.26Cu0.03Co0.03Mo0.03. Under conditions of routine cultivation, trace metal homeostasis may be maintained by a series of transporter systems that are energized by the cell. In specific environments where heavy metals are present at toxic levels, some bacteria have developed a detoxification strategy where the metallic ion is reduced outside of the cell. The result of this extracellular metabolism is that the bacterial metallome specific for trace metals is not disrupted. One of the microorganisms that reduces toxic metals outside of the cell is the sulfate-reducing bacterium Desulfovibrio desulfuricans. While D. desulfuricans reduces metals by enzymatic processes involving polyhemic cytochromes c 3 and hydrogenases, which are all present inside the cell; we report the presence of chain B cytochrome c nitrite reductase, NrfA, in the outer membrane fraction of D. desulfuricans ATCC 27774 and discuss its activity as a metal reductase.

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

Similar content being viewed by others

References

  • Almeida MG, Macieira S, Goncalves LL, Huber R, Cunha CA, Romao MJ, Costa C, Lampreia J, Moura JJ, Moura I (2003) The isolation and characterization of cytochrome c nitrite reductase subunits (NrfA and NrfH) from Desulfovibrio desulfuricans ATCC 27774. Re-evaluation of the spectroscopic data and redox properties. Eur J Biochem 270:3904–3915

    Article  PubMed  CAS  Google Scholar 

  • Anders E, Grevesse N (1989) Abundances of the elements: meteoritic and solar. Geochin Cosmochim Acta 53:197–214

    Article  CAS  Google Scholar 

  • Barton LL (2005) Structural and functional relationships in prokaryotes. Springer, New York

    Google Scholar 

  • Barton LL, Plunkett RM, Thomson BM (2003) Reduction of metals and nonessential elements by anaerobes. In: Ljungdahl LG, Adams MW, Barton LL, Ferry JG, Johnson KK (eds) Biochemistry and physiology of anaerobic bacteria. Springer-Verlag, New York, pp 220–234

    Chapter  Google Scholar 

  • Bencheikh-Latmani R, Williams SM, Haucke L, Criddle CS, Wu L, Zhou J, Tebo BM (2005) Global transcriptional profiling of Shewanella oneidensis MR-1 during Cr(VI) reduction. Appl Environ Microbiol 71:7453–7460

    Article  PubMed  CAS  Google Scholar 

  • Bohnke R, Matzanke BF (1995) The mobile ferrous iron pool in Escherichia coli is bound to a phosphorylated sugar derivative. Biometals 8:223–230

    Article  PubMed  CAS  Google Scholar 

  • Bond DR, Lovley DR (2003) Electrode production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555

    Article  PubMed  CAS  Google Scholar 

  • Bragg JG, Thomas D, Baudouin-Cornu P (2005) Variation among species in proteomic sulfur content is related to environmental conditions. Proc R Soc B 273:1293–1300

    Article  CAS  Google Scholar 

  • Braun V, Hantke K (2001) Mechanisms of bacterial iron transport. In: Winkelmann G (ed) Microbial transport systems. Wiley-VCH, New York, pp 289–311

    Chapter  Google Scholar 

  • Bruschi M (1994) Cytochrome c 3 (Mr 26000) isolated from sulfate-reducing bacteria and its relationships to other polyhemic cytochromes from Desulfovibrio. Meth Enzymol 243:140–155

    Article  PubMed  CAS  Google Scholar 

  • Bruschi M, Barton LL, Goulhen F, Plunkett RM (2006) Enzymatic and genomic studies on the reduction of mercury and selected metallic oxy-anions by sulphate-reducing bacteria. In: Barton LL, Hamilton WA (eds) Sulphate-reducing bacteria: environmental and laboratory activities. Cambridge University Press, Cambridge, UK (In Press)

    Google Scholar 

  • Cartron ME, Maddocks S, Gillingham P, Craven CJ, Andrews SC (2006) Feo - transport of ferrous iron into bacteria. BioMetals 19:143–157

    Article  PubMed  CAS  Google Scholar 

  • Cellier M (2001) Bacterial Genes controlling manganese accumulation. In: Winkelmann G (ed) Microbial Transport Systems. Wiley-VCH, New York, pp 325–346

    Chapter  Google Scholar 

  • Chang IS, Moon H, Bretschger O, Jang JK, Park HI, Nealson KH, Kim BH (2006) Electrochemically active bacteria (EAB) and mediator-less microbial fuel cells. J Microbiol Biotechnol 16:163–177

    CAS  Google Scholar 

  • Chardin B, Giudici-Orticoni MT, De Luca G, Guigliarelli B, Bruschi M (2003) Hydrogenases in sulfate-reducing bacteria function as chromium reductases. Appl Microbiol Biotechnol 63:315–321

    Article  PubMed  CAS  Google Scholar 

  • De Luca G, De Philip P, Dermoun Z, Rousset M, Vermeglio A (2001) Reduction of technetium (VII) by Desulfovibrio fructosorans is mediated by the nickel-iron hydrogenase. Appl Environ Microbiol 67:4583–4587

    Article  PubMed  Google Scholar 

  • Ehrlich HL (1996) Geomicrobiology. Marcel Dekker, New York

    Google Scholar 

  • Eitinger T (2001) Microbial nickel transport. In: Winkelmann G (ed) Microbial transport systems. Wiley-VCH, New York, pp 397–417

    Chapter  Google Scholar 

  • Field SJ, Dobbin PS, Cheesman MR, Watmough NJ, Thomson AJ, Richardson DJ (2000) Purification and magneto-optical spectroscopic characterization of cytoplasmic membrane and outer membrane multiheme c-type cytochromes from Shewanella frigidimarina NCIMB400. J Biol Chem 275:8515–8522

    Article  PubMed  CAS  Google Scholar 

  • Florens L, Bruschi M (1994) Recent advances in the characterization of the hexadecahemic cytochrome c from Desulfovibrio. Biochimie 76:561–568

    Article  PubMed  CAS  Google Scholar 

  • Fraústo da Silva JJR, Williams RJP (2001) The Biological Chemistry of the Elements. Oxford University Press, Inc., New York

    Google Scholar 

  • Gaspard S, Vazquez F, Hollinger C (1998) Localization and solbuilization of the Fe(III) reductase of Geobacter sulfurreducens. Appl Environ Microbiol 64:3188–3194

    PubMed  CAS  Google Scholar 

  • Gordon EHJ, Pike AD, Hill AE, Cuthbertson PM, Chapman SK, Reid GA (2000) Identification and characterization of a novel cytochrome c 3 from Shewanella frigidimarina that is involved in Fe(III) respiration. Biochem J 349:153–158

    Article  PubMed  CAS  Google Scholar 

  • Goulhen F, Gloter A, Guyot F, Bruschi M (2006) Cr(VI) detoxification using sulfate-reducing bacteria: microbe-metal interactions. Appl Microbiol Biotechnol (In Press)

  • Hantke K (2001) Bacterial zinc transport. In: Winkelmann G (ed) Microbial transport systems. Wiley-VCH, New York, pp 313–324

    Chapter  Google Scholar 

  • Ho T-Y, Quigg A, Finkel ZV, Milligan AJ, Wyman K, Falkowski PG, Morel FMM (2003) The elemental composition of some marine phytoplankton. J Phycol 39:1145–1159

    Article  CAS  Google Scholar 

  • Hughes MN, Poole RK (1998) Metals and Micro-organisms. Chapman & Hall, New York

    Google Scholar 

  • Kim BH, Kim HJ, Hyun MS, Park DH (1999) Direct electrode reaction of Fe(III) reducing bacterium, Shewanella putrefaciens. J Microbiol Biotechnol 9:127–131

    Google Scholar 

  • Kim HJ, Park HS, Hyun MS, Chang IS, Kim M, Kim BH (2002) A mediator-less microbial fuel cell using a metal reducing bacterium, Shewanella putrefaciens. Enz Microb Technol 30:125–152

    Article  Google Scholar 

  • Laishley EJ, Bryant RD (2003) Electron flow in ferrous biocorrosion. In: Ljungdahl LG, Adams MW, Barton LL, Ferry JG, Johnson KK (eds) Biochemistry and physiology of anaerobic bacteria. Springer-Verlag, New York, pp 252–260

    Chapter  Google Scholar 

  • Ledrich M-L, Stemmler S, Laval-Gilly P, Foucaud P, Falla J (2005) Precepitation of silver-thiosulfate complex and immobilization of silver by Cupriavidus metallidurans CH34. BioMetals 18:643–650

    Article  PubMed  CAS  Google Scholar 

  • Lloyd JR, Yong P, Macaskie LE (1998) Enzymatic recovery of elemental palladium by using sulfate-reducing bacteria. Appl Environ Microbiol 64:4607–4609

    PubMed  CAS  Google Scholar 

  • Lloyd JR, Ridley J, Khizniak T, Lyalikova NN, Macaskie LE (1999) Reduction of technecium by Desulfovibrio desulfuricans: biocatalyst characterization and use in a flow through bioreactor. Appl Environ Microbiol 65:2691–2696

    PubMed  CAS  Google Scholar 

  • Lloyd JR, Mabbett AN, Williams DR, Macaskie LE (2001) Metal reduction by sulphate-reducing bacteria: physiological diversity and metal specificity. Hydrometallurgy 59:327–337

    Article  CAS  Google Scholar 

  • Lojou E, Bianco P, Bruschi M (1998a) Kinetic studies on the electron transfer between bacterial c-type cytochromes and metal oxides. J Electroanal Chem 452:167–177

    Article  CAS  Google Scholar 

  • Lojou E, Bianco P, Bruschi M (1998b) Kinetic studies on the electron transfer between various c-type cytochromes and iron (III) using voltametric approach. Electrochem Acta 43:2005–2013

    Article  CAS  Google Scholar 

  • Lovley DR (2000) Fe(III) and Mn(IV) reduction. In: Lovley DR (ed) Environmental microbe-metal interactions. ASM Press, Washington, DC; pp 3–30

    Google Scholar 

  • Lovley DR, Phillips EJP (1994) Reduction of chromate by Desulfovibrio vulgaris and its c 3 cytochrome. Appl Environ Microbiol 60:726–728

    PubMed  CAS  Google Scholar 

  • Lovley RD, Widman PK, Woodward JC, Phillips EJP (1993) Reduction of uranium by cytochrome c 3 of Desulfovibrio vulgaris. Appl Environ Microbiol 59:3572–3576

    PubMed  CAS  Google Scholar 

  • Marshall MJ, Elias DA, Kennedy DW, Dohnalkova A, Saffarini DA, Gorby YA, Lipton MS, Beliaev AS, Fredrickson JK (2004) Characterization of uranium (VI) reduction deficiency in a general secretion pathway mutant of Shewanella oneidensis MR-1. American Society for Microbiology General Meeting, New Orleans, May 25, 2004. Abstract Q-159 p 533

  • Michel C, Brugna M, Albert C, Bernadac A, Bruschi M (2001) Enzymatic reduction of chromate: comparative studies using sulfate-reducing bacteria. Key role of polyheme cytochromes c and hydrogenases. Appl Microbiol Biotechnol 55:95–100

    Article  PubMed  CAS  Google Scholar 

  • Moura JJG, Gonzales P, Moura I, Fauque G (2006) Dissimilatory nitrate and nitrite ammonification by sulfate-reducing eubacteria. In: Barton LL, Hamilton WA (eds) Sulphate-reducing bacteria: environmental and laboratory activities. Cambridge University Press, Cambridge, UK. (In Press)

    Google Scholar 

  • Myers JM, Antholine WE, Myers CR (2004) Vanadium (V) reduction by Shewanella oneidensis MR-1 requires menaquinone and cytochromes from the cytoplasmic and outer membranes. Appl Environ Microbiol 70:1405–1412

    Article  PubMed  CAS  Google Scholar 

  • Myers CR, Myers JM (1997) Outer membrane cytochromes of Shewanella putrefaciens MR-1 spectral analysis, and purification of the 83-kDa c-type cytochrome. Biochem Biophys Acta 1326:307–318

    Article  PubMed  CAS  Google Scholar 

  • Myers JM, Myers CR (2001) Role of outer membrane cytochromes OmcA and OmcB of Shewanella putrefaciens MR-1 in reduction of manganese dioxide. Appl Environ Microbiol 67:260–269

    Article  PubMed  CAS  Google Scholar 

  • Myers JM, Myers CR (2003) Overlaping role of the outer membrane cytochromes of Shewanella oneidensis MR-1 in the reduction of manganese (IV) oxide. Lett Appl Microbiol 37:21–25

    Article  PubMed  CAS  Google Scholar 

  • Ohtake H, Cervantes C., Silver S (1987) Decreased chromate uptake in Pseudomonas fluorescens carrying a chromate resistance plasmid. J Bacteriol 169:3853–3856

    PubMed  CAS  Google Scholar 

  • Outten CE, O’Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488–2492

    Article  PubMed  CAS  Google Scholar 

  • Pau RN, Klipp W, Limkhler S (1997) Molybdenum transport, processing and gene regulation. In: Winkelmann G, Carrano CJ Jr. (eds) Transition metals in microbial metabolism. Harwood Academic, Amsterdam, pp 217–234

    Google Scholar 

  • Reguera G, McCarthy KD, Mehta T, Nicoll SS, Tuominen MT, Lovley DR (2005) Extracellular electron transfer via microbial nanowires. Nature 435:1098–1101

    Article  PubMed  CAS  Google Scholar 

  • Solioz M (2001) Bacterial copper transport. In: Winkelmann G (ed) Microbial transport systems. Wiley-VCH, New York, pp 361–376

    Chapter  Google Scholar 

  • Rodrigue ML, Oliveira T, Matias PM, Martins IC, Valente FM, Pereira IA, Archer M (2006) Crystallization and preliminary structure determination of the membrane-bound complex cytochrome c nitrite reductase from Desulfovibrio vulgaris Hildenborough. Acta Crystallograph Sect F Struct Biol Cryst Commun 62:565–568

    Article  CAS  Google Scholar 

  • Romao CV, Regalla M, Xavier AV, Teixeira M, Liu MY, LeGall J (2000) A bacterioferritin from the strict anaerobe Desulfovibrio desulfuricans ATCC 27774. Biochem 39:6841–6849

    Article  CAS  Google Scholar 

  • Shcolnick S, Keren N (2006) Metal homeostasis in cyanobacteria and chloroplasts, balancing benefits and risks to the photosynthetic apparatus. Plant Physiol 141:805–810

    Article  PubMed  CAS  Google Scholar 

  • Silver S, Phung LT (1996) Bacterial heavy metal resistances. Ann Rev Microbiol 50:753–789

    Article  CAS  Google Scholar 

  • Smith RJ (1995) Calcium and bacteria. Adv Microbial Physiol 37:83–133

    Article  CAS  Google Scholar 

  • Strumm W, Morgan JJ (1996) Aquatic Chemistry. 3rd edn. John Wiley & Sons, Inc., New York

    Google Scholar 

  • Tomei FA, Barton LL, Lemanski CL, Zocco TG, Fink NH, Sillerud LO (1995) Transformation of selenate and selenite to elemental selenium by Desulfovibrio desulfuricans. J Indust Microbiol 14:329–336

    Article  CAS  Google Scholar 

  • Tucker MD, Barton LL, Thomson BM (1996) Kinetic coefficients for simultaneous reduction of slulfate and uranium by Desulfovibrio desulfuricans. Appl Microbiol Biotechnol 46:74–77

    Article  CAS  Google Scholar 

  • Tucker MD, Barton LL, Thomson BM (1997) Reduction and immobilization of molybdate by Desulfovibrio desulfuricans. J Environ Quality 26:1146–1152

    Article  CAS  Google Scholar 

  • Tucker MD, Barton LL, Thomson BM (1998) Reduction of Cr, Mo, Se and U by Desulfovibrio desulfuricans immobilized in polyacrylamide gels. J Ind Microbiol Biotechnol 20:13–19

    Article  PubMed  CAS  Google Scholar 

  • Turner SM., Moir JWB, Griffiths L, Overton TW, Smith H, Cole JA (2005) Mutational and biochemical analysis of cytochrome c’ a nitric oxide binding lipoprotein important for adaption of Neisseria gonorrhoeae to oxygen-limited growth. Biochem J 388:545–553

    Article  PubMed  CAS  Google Scholar 

  • Van Ommen Kloeke F, Bryant RD, Laishley EJ (1995) Localization of cytochromes in the outer membrane of Desulfovibrio vulgaris (Hildenborough) and their role in anaerobic biocorrosion. Anaerobe 1:351–358

    Article  PubMed  Google Scholar 

  • Volesky B (ed) (1990) Biosorption of Heavy Metals. CRC Press, Boca Raton, FL

  • Wackett LP, Orme-Johnson WH, Walsh CT (1989) Transition metal enzymes in bacterial metabolism. In: Beveridge TJ, Doyle RJ (eds) Metal ions and bacteria. John Wiley & Sons, New York, pp 165–206

    Google Scholar 

  • Wall J, Yen HCB, Drury EC (2006) Evaluation of stress response in sulphate-reducing bacteria through genome analysis. In: Barton LL, Hamilton WA (eds) Sulphate-reducing bacteria: environmental and laboratory activities. Cambridge University Press, Cambridge, UK. (In Press)

    Google Scholar 

  • Xu H, Barton LL, Zhang P, Wang Y (2000) TEM investigation of U6+ and Re7+ reduction by Desulfovibrio desulfuricans, a sulfate reducing bacterium. Sci Basis for Nucl Waste Manage 23:361–371

    Google Scholar 

Download references

Acknowledgment

This work was supported, in part, by grants from US DOE and the US Army. NAW was supported by MARC and IMSD grants from National Institute of Health.

Author information

Authors and Affiliations

  1. Department of Biology, Laboratory of Microbial Chemistry, University of New Mexico, MSC03 2020, Albuquerque, NM, 87131-0001, USA

    Larry L. Barton, Nicole A. Woodards & Richard M. Plunkett

  2. Institut de Biologie Structurale et Microbiologie, Unité de Bioénergétique et Ingénierie des Protéines, CNRS, 31 chemin Joseph Aiguier, Marseille cedex 20, 13402, France

    Florence Goulhen & Mireille Bruschi

  3. Department of Earth and Planetary Sciences, University of New Mexico, Albuquerque, NM, 87131-0001, USA

    Frans J. M. Rietmeijer

Authors
  1. Larry L. Barton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Florence Goulhen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mireille Bruschi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nicole A. Woodards
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Richard M. Plunkett
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Frans J. M. Rietmeijer
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Larry L. Barton.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barton, L.L., Goulhen, F., Bruschi, M. et al. The bacterial metallome: composition and stability with specific reference to the anaerobic bacterium Desulfovibrio desulfuricans . Biometals 20, 291–302 (2007). https://doi.org/10.1007/s10534-006-9059-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10534-006-9059-2

Keywords

Search

Navigation