Skip to main content
SpringerLink
Log in

Biological characterization of lead-enhanced exopolysaccharide produced by a lead resistant Enterobacter cloacae strain P2B

  • Original Paper
  • Published:
Biodegradation Aims and scope Submit manuscript

Abstract

A lead resistant bacterial strain isolated from effluent of lead battery manufacturing company of Goa, India has been identified as Enterobacter cloacae strain P2B based on morphological, biochemical characters, FAME profile and 16S rDNA sequence data. This bacterial strain could resist lead nitrate up to 1.6 mM. Significant increase in exopolysaccharide (EPS) production was observed as the production increased from 28 to 108 mg/L dry weight when exposed to 1.6 mM lead nitrate in Tris buffered minimal medium. Fourier-transformed infrared spectroscopy of this EPS revealed presence of several functional groups involved in metal binding viz. carboxyl, hydroxyl and amide groups along with glucuronic acid. Gas chromatography coupled with mass spectrometry analysis of alditol-acetate derivatives of acid hydrolysed EPS produced in presence of 1.6 mM lead nitrate demonstrated presence of several neutral sugars such as rhamnose, arabinose, xylose, mannose, galactose and glucose, which contribute to lead binding hydroxyl groups. Scanning electron microscope coupled with energy dispersive X-ray spectrometric analysis of this lead resistant strain exposed to 1.6 mM lead nitrate interestingly revealed mucous EPS surrounding bacterial cells which sequestered 17 % lead (as weight %) extracellularly and protected the bacterial cells from toxic effects of lead. This lead resistant strain also showed multidrug resistance. Thus these results significantly contribute to better understanding of structure, function and environmental application of lead-enhanced EPSs produced by bacteria. This lead-enhanced biopolymer can play a very important role in bioremediation of several heavy metals including lead.

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

  • Albersheim P, Nevins DJ, English PD, Karr A (1967) A method for the analysis of sugars in plant cell-wall polysaccharides by gas-liquid chromatography. Carbohydr Res 5:340–345

    Article  CAS  Google Scholar 

  • Altchul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  Google Scholar 

  • Arias S, del Moral A, Ferrer MR, Quesada RTE, Bejar V (2003) Mauran, an exopolysaccharide produced by the halophilic bacterium Halomonas maura, with a novel composition and interesting properties for biotechnology. Extremophiles 7:319–326

    Article  PubMed  CAS  Google Scholar 

  • Asmub M, Mullenders LHF, Hartwig A (2000) Interference by toxic metal compounds with isolated zinc finger DNA repair proteins. Toxicol Lett 112:227–231

    Article  Google Scholar 

  • Baker-Austin C, Wright MS, Stepanauskas R, McArthur JV (2006) Co-selection of antibiotic and metal resistance. Trends Microbiol 14:176–182

    Article  PubMed  CAS  Google Scholar 

  • Bauer AW, Kirby WMM, Sherris JC, Turck M (1966) Antibiotic susceptibility testing by a standardized single disc method. Am J Clin Pathol 45:493–496

    PubMed  CAS  Google Scholar 

  • Bhaskar PV, Bhosle NB (2005) Microbial extracellular polymeric substances in marine biogeochemical processes. Curr Sci 88:45–53

    CAS  Google Scholar 

  • Bhaskar PV, Bhosle NB (2006) Bacterial extracellular polymeric substances (EPS) a carrier of heavy metals in the marine food-chain. Environ Int 32:192–198

    Article  Google Scholar 

  • Bramhachari P, Dubey SK (2006) Isolation and characterization of exopolysaccharide produced by Vibrio harveyi VB23. Lett Appl Microbiol 43:571–577

    Article  PubMed  CAS  Google Scholar 

  • Bramhachari PV, Kavi Kishor PB, Ramadevi R, Kumar R, Rao BR, Dubey SK (2007) Isolation and characterization of mucous exopolysaccharide produced by Vibrio furnissii VB0S3. J Microbiol Biotechnol 17:44–51

    PubMed  CAS  Google Scholar 

  • Decho AW (1990) Microbial exopolymer secretion in ocean environment, their roles in food webs and marine processes. Oceanogr Mar Biol Annu Rev 28:73–153

    Google Scholar 

  • Dirilgen N (2011) Mercury and lead: assessing the toxic effects on growth and metal accumulation by Lemna minor. Ecotoxicol Environ Saf 74:48–54

    Article  PubMed  CAS  Google Scholar 

  • Fernandes N, Beiras R (2001) Combined toxicity of dissolved mercury with copper, lead and cadmium on embryogenesis and early larval growth of the Paracentrotus lividus sea-urchin. Ecotoxicology 10:263–271

    Article  Google Scholar 

  • Fowler BA (1998) Role of lead binding proteins in mediating lead bioavailability. Environ Health Perspect 106:1585–1587

    Article  PubMed  CAS  Google Scholar 

  • Fox A, Morgan SL, Gilbart J (1988) Preparation of alditol acetates and their analysis by gas chromatography and mass spectrometry. In: Bierman CJ, McGinnis G (eds) Analysis of carbohydrates by GLC and MS. CRC Press, Boca Raton, pp 87–117

    Google Scholar 

  • Hartwig A, Asmuss M, Ehleben I, Herzer U, Kostelac D, Pelzer A, Schwerdtle T, Burkle A (2002) Interference by toxic metal ions with DNA repair processes and cell cycle control: molecular mechanisms. Environ Health Perspect 110:797–799

    Article  PubMed  CAS  Google Scholar 

  • Iyer A, Mody K, Jha B (2004) Accumulation of hexavalent chromium by an exopolysaccharide producing marine Enterobacter cloaceae. Mar Pollut Bull 49:974–977

    Article  PubMed  CAS  Google Scholar 

  • Krieg NR, Holt JG (1984) Bergey’s manual of systematic bacteriology, vol I. The Williams and Wilkins, Baltimore, pp 140–309

    Google Scholar 

  • Lam TV, Agovino P, Niu X, Roche L (2007) Linkage study of cancer risk among lead exposed workers in New Jersey. Sci Total Environ 372:455–462

    Article  PubMed  CAS  Google Scholar 

  • Mergeay M, Nies DH, Schlegel HG, Gerits J, Charles P, Van Gijsegem F (1985) Alcaligenes eutrophus CH34 is a facultative chemolithotroph with plasmid-bound resistance to heavy metals. J Bacteriol 162:328–334

    PubMed  CAS  Google Scholar 

  • Morillo JA, Aguilera M, Ramoz-Cormenzana A, Monteoliva SM (2006) Production of metal-binding exopolysaccharide by Paenibacillus jamilae using two-phase olive-mill waste as fermentation substrate. Curr Microbiol 53:189–193

    Article  PubMed  CAS  Google Scholar 

  • Naik MM, Dubey SK (2011) Lead-enhanced siderophore production and alteration in cell morphology in a Pb-resistant Pseudomonas aeruginosa strain 4EA. Curr Microbiol 62:409–414

    Article  PubMed  CAS  Google Scholar 

  • Nies DH (1999) Microbial heavy-metal resistance. Appl Microbiol Biotechnol 51:730–750

    Article  PubMed  CAS  Google Scholar 

  • Ozturk S, Aslim B, Ugur A (2008) Chromium(VI) resistance and extracellular polysaccharide (EPS) synthesis by Pseudomonas, Stenotrophomonas and Methylobacterium strains. ISIJ Int 48:1654–1658

    Article  CAS  Google Scholar 

  • Ozturk S, Aslim B, Suludere Z (2010) Cadmium(II) sequestration characteristics by two isolates of Synechocystis sp. in terms of exopolysaccharide (EPS) production and monomer composition. Bioresour Technol 101:9742–9748

    Article  PubMed  CAS  Google Scholar 

  • Pal A, Paul AK (2008) Microbial extracellular polymeric substances: central elements in heavy metal bioremediation. Indian J Microbiol 48:49–64

    Article  CAS  Google Scholar 

  • Roane TM (1999) Lead resistance in two bacterial isolates from heavy metal-contaminated soils. Microb Ecol 37:218–224

    Article  PubMed  CAS  Google Scholar 

  • Royan S, Parulekar C, Mavinkurve S (1999) Exopolysaccharides of Pseudomonas mendocina P2d. Lett Appl Microbiol 29:342–346

    Article  CAS  Google Scholar 

  • Sinha A, Khare SK (2011) Mercury bioremediation by mercury accumulating Enterobacter sp. cells and its alginate immobilized application. Biodegradation. doi:.1007/s10532-011-9483-z

    PubMed  Google Scholar 

  • Taghavi S, Lesaulnier C, Monchy S, Wattiez R, Mergeay M, van der Lelie D (2009) Lead (II) resistance in Cupriavidus metallidurans CH34: interplay between plasmid and chromosomally-located functions. Antonie Van Leeuwenhoek 96:171–182

    Article  PubMed  CAS  Google Scholar 

  • Tong S, von Schirnding YE, Prapamontol T (2000) Environmental lead exposure: a public health problem of global dimensions. Bull World Health Organ 78:1068–1077

    PubMed  CAS  Google Scholar 

  • van Hullebusch ED, Zandvoort MH, Lens PNL (2003) Metal immobilisation by biofilms: mechanisms and analytical tools. Rev Environ Sci Biotechnol 2:9–33

    Article  Google Scholar 

  • Watt GCM, Britton A, Gilmour HG, Moore MR, Murray GD, Robertson SJ (2000) Public health implications of new guidelines for lead in drinking water: a case study in an area with historically high water lead levels. Food Chem Toxicol 38:73–79

    Google Scholar 

  • Yin Y, Hu Y, Xiong F (2011) Sorption of Cu(II) and Cd(II) by extracellular polymeric substances (EPS) from Aspergillus fumigates. I. Int Biodeterior Biodegrad 65:1012–1018

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Milind Naik gratefully acknowledges UGC, Government of India for financial support as Junior Research Fellowship. The authors are also thankful to Dr. M. S. Prasad and Mr. Vijay Khedekar from National Institute of Oceanography, Goa, India for scanning electron microscopy.

Author information

Authors and Affiliations

  1. Laboratory of Bacterial Genetics and Environmental Biotechnology, Department of Microbiology, Goa University, Taleigao Plateau, Panaji, 403 206, Goa, India

    Milind Mohan Naik, Anju Pandey & Santosh Kumar Dubey

Authors
  1. Milind Mohan Naik
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Anju Pandey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Santosh Kumar Dubey
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Santosh Kumar Dubey.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 95 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Naik, M.M., Pandey, A. & Dubey, S.K. Biological characterization of lead-enhanced exopolysaccharide produced by a lead resistant Enterobacter cloacae strain P2B. Biodegradation 23, 775–783 (2012). https://doi.org/10.1007/s10532-012-9552-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10532-012-9552-y

Keywords

Search

Navigation