Skip to main content
SpringerLink
Log in

Isolation and identification of a bacterium with high tolerance to lead and copper from a marine microbial mat in Spain

  • Original Article
  • Published:
Annals of Microbiology Aims and scope Submit manuscript

Abstract

A bacterial strain (DE2008) was isolated from a consortium of microorganisms living in the microbial mats of the Ebro Delta with the ability to grow under conditions of high concentrations of lead and copper. Strain DE2008 has been characterized by microscopic and metabolic techniques and identified by sequencing of PCR-amplified 16S rRNA gene fragments as Micrococcus luteus. The strain is highly resistant to lead and copper. Micrococcus luteus DE2008 grew optimally until levels of 1 mM of Pb(NO3)2 and CuSO4, respectively, and was completely inhibited at 3 mM Pb(NO3)2 and at 1.5 mM CuSO4. Elemental analysis determined by energy-dispersive X-ray spectroscopy (EDX) coupled with scanning electron microscopy and transmission electron microscopy from polluted cultures of DE2008 show that this microorganism can biosorpt Pb and Cu in exopolysaccharide envelopes, without accumulating them inside the cells.

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
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Al-Hasan RH, Al-Bader D, Sorkhoh NA, Radwan SS (1998) Evidence for n-alakane consumption and oxidation by filamentous cyanobacteria from oil-contaminated coasts of the Arabian Gulf. Mar Biol 130:521–527

    Article  CAS  Google Scholar 

  • Bamji MS, Krinsky NI (1966) The carotenoid pigments of a radiation-resistant Micrococcus species. Biochim Biophys Acta 2:276–284

    Google Scholar 

  • Binupriya AR, Sathishkumar M, Swaminathan K, Jeong ES, Yun SE, Pattabi S (2006) Biosorption of metal ions from aqueous solution and electroplating industry wastewater by Aspergillus japonicus: phytotoxicity studies. Bull Environ Contam Toxicol 2:219–227

    Article  CAS  Google Scholar 

  • Bordenave S, Fourçans A, Blachard S, Goño MS, Caumette P, Duran P (2004) Structure and functional analysis of bacterial communities changes in microbial mats following petroleum exposure. Ophelia 58:195–203

    Google Scholar 

  • Burnat M, Diestra E, Esteve I, Solé A (2009) Confocal laser scanning microscopy coupled to a spectrofluorometric detector as a rapid tool for determining the in vivo effect of metals on phototrophic bacteria. Bull Environ Contam Toxicol. doi:10.1007/s00128-009-9907-1

    PubMed  Google Scholar 

  • Chaudri AM, Celine G, Allain Vl, Barbosa-Jefferson FA, Nicholson BJ, Chambers SP, McGrath A (2000) A study of the impacts of Zn and Cu on two rhizobial species in soils of a long-term field experiment. Plant Soil 221:167–179

    Article  CAS  Google Scholar 

  • Cowan ST, Steel KJ (1965) Manual for the identification of medical bacteria. Cambridge University Press, New York

    Google Scholar 

  • Decho AW (1994) Exopolymers in microbial mats: assessing their adaptative roles. In: Stal LJ, Caumette P (eds) Microbial mats. Structure, developement and environmental significance. Springer, Berlin, pp 215–219

    Google Scholar 

  • Diestra E, Solé A, Esteve I (2004) A comparative study of cyanobacterial diversity in polluted and unpolluted microbial mats by means of CLSM. Ophelia 58:151–156

    Google Scholar 

  • Diestra E, Solé A, Martí M, García de Oteyza T, Grimalt JO, Esteve I (2005) Characterization of an oil-degrading Microcoleus consortium by means of confocal scanning microscopy, scanning electron microscopy and transmission electron microscopy. Scanning 4:176–180

    Google Scholar 

  • Doddamani HP, Ninnekar HZ (2001) Biodegradation of carbaryl by a Micrococcus species. Curr Microbiol 1:69–73

    Article  Google Scholar 

  • García de Oteyza T, Grimalt JO, Diestra E, Solé A, Esteve I (2004) Changes in the composition of polar and apolar crude oil fractions under the action of Microcoleus consortia. Appl Microbiol Biotechnol 2:226–232

    Article  CAS  Google Scholar 

  • Goldberg J, González H, Jensen TE, Corpe WA (2001) Quantitative analysis of the elemental composition and the mass of bacterial polyphosphate bodies using STEM EDX. Microbios 415:177–188

    Google Scholar 

  • Gong R, Ding Y, Liu H, Chen Q, Liu Z (2005) Lead biosorption and desorption by intact and pretreated Spirulina maxima biomass. Chemosphere 1:125–130

    Article  CAS  Google Scholar 

  • Greenblatt CL, Baum J, Klein BY, Nachshon S, Koltunov V, Cano RJ (2004) Micrococcus luteus—survival in amber. Microb Ecol 1:120–127

    Article  Google Scholar 

  • Jensen TE, Sicko LM (1974) Phosphate metabolism in blue-green algae. I. Fine structure of the “polyphosphate overplus” phenomenon in Plectonema boryanum. Can J Microbiol 9:1235–1239

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of proteins molecules. In: Munro HR (ed) Mammalian proteins metabolism. Academic, New York, pp 21–23

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 2:150–163

    Article  Google Scholar 

  • Nakajima A, Tsuruta T (2004) Competitive biosorption of thorium and uranium by Micrococcus luteus. J Radioanal Nucl Chem 260:13–18

    Article  CAS  Google Scholar 

  • Radwan SS, Sorkhoh NA (1993) Lipids of n-alkanes ultilizing microorganisms and their application potential. Adv Appl Microbiol 39:29–90

    Article  CAS  Google Scholar 

  • Roane TM, Pepper IL (2000) Microorganisms and metal pollutants. In: Maier RM, Pepper IL, Gerba CP (eds) Environmental microbiology, Academic, New York, pp 403–423

  • Roy S, Ghosh AN, Thakur AR (2008) Uptake of Pb(2+)by a cyanobacterium belonging to the genus Synechocystis, isolated from East Kolkata Wetlands. Biometals 5:515–524

    Article  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Sánchez O, Diestra E, Esteve I, Mas J (2005) Molecular characterization of an oil-degrading cyanobacterial consortium. Microb Ecol 4:580–588

    Article  CAS  Google Scholar 

  • Sánchez-Chardi A, López-Fuster MJ, Nadal J (2007) Bioaccumulation of lead, mercury, and cadmium in the greater white-toothed shrew, Crocidura russula, from the Ebro Delta (NE Spain): sex- and age-dependent variation. Environ Pollut 1:7–14

    Article  CAS  Google Scholar 

  • Sicko LM (1972) Structural variation of polyphosphate bodies in blue-green algae. In: Arceneaux J (ed) 30th Annual Proceedings of the Electron Microscope Society of America. Los Angeles, pp 218–219

  • Sims GK, Sommers LE, Konopka A (1986) Degradation of pyridine by micrococcus luteus isolated from soil. Appl Environ Microbiol 5:963–968

    Google Scholar 

  • Solé A, Diestra E, Esteve I (2009) Confocal laser scanning microscopy image analysis for cyanobacterial biomass determined at microscale level in different microbial mats. Microb Ecol 4:649–656

    Article  Google Scholar 

  • Stal LJ (2000) Cyanobacterial mats and stromatolites. In: Whitton BA, Potts M (eds) The ecology of cyanobacteria. Kluwer, Dordrecht, pp 61–120

    Google Scholar 

  • Stevens SE Jr, Nierzwicki-Bauer SA, Balkwill DL (1985) Effect of nitrogen starvation on the morphology and ultrastructure of the cyanobacterium Mastigocladus laminosus. J Bacteriol 3:1215–1218

    Google Scholar 

  • Takeuchi M, Weiss N, Schumann P, Yokota A (1996) Leucobacter komagatae gen. nov., sp. nov., a new aerobic Gram-positive, nonsporulating rod with 2, 4-diaminobutyric acid in the cell wall. Int J Syst Bacteriol 4:967–971

    Article  Google Scholar 

  • Tallur PN, Megadi VB, Ninnekar HZ (2008) Biodegradation of cypermethrin by Micrococcus sp. strain CPN 1. Biodegradation 1:77–82

    Article  CAS  Google Scholar 

  • Tunali S, Çabu A, Akar T (2006) Removal of lead and copper ions from aqueous solutions by bacterial strain isolated from soil. Chem Eng J 115:203–211

    Article  CAS  Google Scholar 

  • Wang YC (2005) Study on kinetics of alcohol fermentation on the basis of the biomass specific growth rate. Liq Sci Technol 9:48–51

    Google Scholar 

  • Wei G, Fan L, Zhu W, Fu Y, Yu J, Tang M (2009) Isolation and characterization of the heavy metal resistant bacteria CCNWRS33-2 isolated from root nodule of Lespedeza cuneata in gold mine tailings in China. J Hazard Mater 1:50–56

    Article  CAS  Google Scholar 

  • Zhuang WQ, Tay JH, Maszenan AM, Krumholz LR, Tay ST (2003) Importance of Gram-positive naphthalene-degrading bacteria in oil-contaminated tropical marine sediments. Lett Appl Microbiol 4:251–257

    Google Scholar 

  • Ziagova M, Dimitriadis G, Aslanidou D, Papaioannou X, Litopoulou TE, Liakopoulou-Kyriakides M (2007) Comparative study of Cd(II) and Cr(VI) biosorption on Staphylococcus xylosus and Pseudomonas sp. in single and binary mixtures. Bioresour Technol 15:2859–2865

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by two Spanish grants DGICYT (Refs. CGL2005-03792/BOS and CGL2008-01891/BOS) and by Generalitat de Catalunya grant ITT-CTP (Ref. 2007ITT 00003). We express our thanks to the staff of the Servei de Microscòpia at the Universitat Autònoma de Barcelona for technical assistance with the electron microscopy. We also thank Marc Alamany and Francesc Fornells from Ecología Portuaria S.L. (Spain), who provided valuable comments on the manuscript. Finally, we acknowledge Cristina Sosa and Pilar Jarque for their help in this work.

Author information

Authors and Affiliations

  1. Department of Genetics and Microbiology, Biosciences Faculty, Universitat Autònoma de Barcelona, Bellaterra, 08193, Barcelona, Spain

    Juan Maldonado, Elia Diestra, Ana M. Domènech, Eduard Villagrasa, Zully M. Puyen, Isabel Esteve & Antonio Solé

  2. Equipe Environnement et Microbiologie, IPREM UMR CNRS 5254, Université de Pau et des Pays de l’Adour, IBEAS, BP 1155, 64013, Pau Cedex, France

    Lionel Huang & Robert Duran

Authors
  1. Juan Maldonado
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elia Diestra
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lionel Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ana M. Domènech
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Eduard Villagrasa
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zully M. Puyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Robert Duran
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Isabel Esteve
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Antonio Solé
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juan Maldonado.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Maldonado, J., Diestra, E., Huang, L. et al. Isolation and identification of a bacterium with high tolerance to lead and copper from a marine microbial mat in Spain. Ann Microbiol 60, 113–120 (2010). https://doi.org/10.1007/s13213-010-0019-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13213-010-0019-2

Keywords

Search

Navigation