Log in

Morphological changes in an acidophilic bacterium induced by heavy metals

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

Abstract

The Acidiphilium strains inhabit acidic mine regions where they are subjected to occasional environmental stresses such as high and low temperatures, exposure to various heavy metals, etc. Change in morphology is one of the strategies that bacteria adopt to cope with environmental stresses; however, no study on this aspect has been reported in the case of Acidiphilium sp. This work is an attempt using the acidophilic heterotrophic bacterium Acidiphilium symbioticum H8. It was observed that the maximum alterations in size occurred when the bacterium was exposed to sub-inhibitory concentrations of Cu and Cd. Loosely packed coccobacillus-type normal cells formed characteristic chains of coccoidal lenticular shape with constrictions at the junctions between them in the presence of Cd; Cu induced transformation of cells to become round shaped; Ni caused the cells to aggregate, but Zn showed no effect. Respective metal depositions on the cell surface were confirmed by scanning electron microscopy equipped with energy dispersive X-ray analysis. Cell bound Ca2+ ions were replaced by these metal ions and measured by inductively coupled plasma mass spectrometry from the culture filtrate. Cell shape changed only after the addition of sub-inhibitory concentrations of the metals, but in growth inhibitory concentrations it was similar to the normal cells.

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

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Baker-Austin C, Dopson M (2007) Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15:165–171

    Article  PubMed  CAS  Google Scholar 

  • Bennet AF, Lenski RF, Mittler JE (1992) Evolutionary adaptation to temperature: 1. Fitness responses of Escherichia coli to changes in its thermal environments. Evolution 46:16–30

    Article  Google Scholar 

  • Bhattacharya S, Chakrabarti BK, Das A, Kundu PN, Banerjee PC (1991) Acidiphilium symbioticum sp.nov., an acidophilic heterotrophic bacterium from Thiobacillus ferrooxidans cultures isolated from Indian mines. Can J Microbiol 37:78–85

    Article  Google Scholar 

  • Brown NL, Rouch DA, Lee BTO (1992) Copper resistance determinants in bacteria. Plasmid 27:41–51

    Article  PubMed  CAS  Google Scholar 

  • Bruins MR, Kapil S, Oehme FW (2000) Microbial resistance to metals in the environment. Ecotoxicol Environ Saf 45:198–207

    Article  PubMed  CAS  Google Scholar 

  • Chakravarty R, Manna S, Ghosh AK, Banerjee PC (2007) Morphological changes in an Acidocella strain in response to heavy metal stress. Res J Microbiol 2:742–748

    Article  CAS  Google Scholar 

  • Costa CS, Anton DN (1999) Conditional lethality of cell shape mutations of Salmonella typhimurium: rodA and mre mutants are lethal on solid but not in liquid medium. Curr Microbiol 38:137–142

    Article  PubMed  CAS  Google Scholar 

  • da Silva ACR, Reinach FC (1991) Calcium binding induces conformational changes in muscle regulatory proteins. Trends Biochem Sci 16:53–57

    Article  PubMed  Google Scholar 

  • Dopson M, Baker-Austin C, Koppineedi PR, Bond PL (2003) Growth in sulfidic mineral environments: metal resistance mechanisms in acidophilic micro-organisms. Microbiol 149:1959–1970

    Article  CAS  Google Scholar 

  • Ehrlich HL, Brierly CL (1990) Microbial mineral recovery. McGraw-Hill, New York

    Google Scholar 

  • Franklin TJ, Snow GA (1981) Biochemistry of antimicrobial action. Chapman & Hall, New York, pp 21–57

    Google Scholar 

  • Gogolev A, Wilke BM (1997) Combination effects of heavy metals and fluoranthene on soil bacteria. Biol Fertil Soils 25:274–278

    Article  CAS  Google Scholar 

  • Hallberg KB, Johnson DB (2001) Biodiversity of acidophilic microorganisms. Adv Appl Microbiol 49:37–84

    PubMed  CAS  Google Scholar 

  • Huheey JE, Keiter EA, Keiter RL (1993) Inorganic chemistry: principles of structure and reactivity, 4th ed. Harper Collins College, New York

    Google Scholar 

  • Ikura M (1996) Calcium binding and conformational response in EF-hand proteins. Trends Biochem Sci 21:14–17

    PubMed  CAS  Google Scholar 

  • Ji G, Silver S (2005) Bacterial resistance mechanisms for heavy metals of environmental concern. J Ind Microbiol Biotechnol 14:61–75

    Google Scholar 

  • Kotra LP, Golemi D, Amro NA, Liu GY, Mobashery S (1999) Dynamics of the lipopolysaccharide assembly on the surface of Escherichia coli. J Am Chem Soc 121:8707–8711

    Article  CAS  Google Scholar 

  • Kuroki R, Taniyama Y, Seko C, Nakamura H, Kikuchi M, Ikehara M (1989) Design and creation of a Ca2+ binding site in human lysozyme to enhance structural stability. Proc Natl Acad Sci 86:6903–6907

    Article  PubMed  CAS  Google Scholar 

  • Lom J, Weiser J (1972) Surface pattern of some microsporidian spore as seen in SEM. Folia Parasitol 19:359–363

    PubMed  CAS  Google Scholar 

  • Mahapatra NR, Banerjee PC (1996) Extreme tolerance to cadmium and high resistance to copper, nickel and zinc in different Acidiphilium strains. Lett Appl Microbiol 23:393–397

    CAS  Google Scholar 

  • Nepple BB, Flynn I, Bachofen R (1999) Morphological changes in phototrophic bacteria induced by metalloid oxyanions. Microbiol Res 154:191–198

    CAS  Google Scholar 

  • Neumann G, Veeranagouda Y, Karegoudar TB, Sahin Ö, Mäusezahl I, Kabelitz N, Kappelmeyer U, Heipieper HJ (2005) Cells of Pseudomonas putida and Enterobacter sp. adapt to toxic organic compounds by increasing their size. Extremophiles 9:163–168

    Article  PubMed  CAS  Google Scholar 

  • Nies DH (1992) Resistance to cadmium, cobalt, zinc, and nickel in microbes. Plasmid 27:17–28

    Article  PubMed  CAS  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  PubMed  CAS  Google Scholar 

  • Peng L, Yi L, Zhexue L, Juncheng Z, Jiaxin D, Daiwen P, ** S, Songsheng Q (2004) Study on biological effect of La3+ on Escherichia coli by atomic force microscopy. J Inorg Biochem 98:68–72

    Article  CAS  Google Scholar 

  • Pidcock E, Moore GR (2001) Structural characteristics of protein binding sites for calcium and lanthanide ions. J Biol Inorg Chem 6:479–489

    Article  PubMed  CAS  Google Scholar 

  • Ramos JL, Gallegos MT, Marques S, Ramos-Gonzalez MI, Espinosa-Urgel M, Sugura A (2001) Responses of Gram-negative bacteria to certain environmental stressors. Curr Opin Microbiol 4:166–171

    Article  PubMed  CAS  Google Scholar 

  • Rawlings DE (2002) Heavy metal mining using microbes. Annu Rev Microbiol 56:65–91

    Article  PubMed  CAS  Google Scholar 

  • Rawlings DE, Silver S (1995) Mining with microbes. Biotechnology 13:773–778

    Article  CAS  Google Scholar 

  • Santamaría MM, Marrero ARD, Hernández J, Navarro AMG, Corzo J (2003) Effect of thorium on the growth and capsule morphology of Bradyrhizobium. Environ Microbiol 5:916–924

    Article  PubMed  CAS  Google Scholar 

  • Shi B, **a X (2003) Morphological changes of Pseudomonas pseudoalcaigenes in response to temperature selection. Curr Microbiol 46:120–123

    Article  PubMed  CAS  Google Scholar 

  • Skelton NJ, Kördel J, Akke M, Forsén S, Chazin WJ (1994) Signal transduction versus buffering activity in Ca2+–binding proteins. Nat Struct Biol 1:239–245

    Article  PubMed  CAS  Google Scholar 

  • Storz G, Hengge-Aronis R (2000) Bacterial stress responses. ASM, Washington

    Google Scholar 

  • Young KD (2003) Bacterial shape. Mol Microbiol 49:571–580

    Article  PubMed  CAS  Google Scholar 

  • Young KD (2006) The selective value of bacterial shape. Microbiol Mol Biol Rev 70:660–703

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the help of Dr. S. Chakraborty, University Science Instrumentation Centre, Burdwan University, West Bengal, and Dr. S. Shome, Geological Survey of India, Kolkata for providing SEM facilities. Many thanks are also addressed to Mrs. S. Shome Mazumder, Institute of Wetland Management and Ecological Design, Kolkata, for her help to conduct AAS experiments successfully. R. Chakravarty thankfully acknowledges the Senior Research Fellowship provided by Council of Scientific and Industrial Research (CSIR), New Delhi.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Pataki C. Banerjee.

Additional information

Communicated by K. Horikoshi.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chakravarty, R., Banerjee, P.C. Morphological changes in an acidophilic bacterium induced by heavy metals. Extremophiles 12, 279–284 (2008). https://doi.org/10.1007/s00792-007-0128-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00792-007-0128-4

Keywords

Navigation