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Research article

Environmental Microbiology and Engineering

Biomineralization of Calcium Carbonate Polymorphs by the Bacterial Strains Isolated from Calcareous Sites

Navdeep Kaur Dhami 1, M. Sudhakara Reddy 1* and Abhijit Mukherjee 2

1Department of Biotechnology, Thapar University, Patiala 147004, India, 2Department of Civil Engineering, Thapar University, Patiala 147004, India

Received: December 3, 2012; Accepted: December 30, 2012

J. Microbiol. Biotechnol. 2013; 23(5): 707-714

Published May 25, 2013 https://doi.org/10.4014/jmb.1212.11087

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Microbially induced calcium carbonate precipitation (MICCP) is a naturally occurring biological process that has various applications in remediation and restoration of a range of building materials. In the present investigation, five ureolytic bacterial isolates capable of inducing calcium carbonate precipitation were isolated from calcareous soils on the basis of production of urease, carbonic anhydrase, extrapolymeric substances, and biofilm. Bacterial isolates were identified as Bacillus megaterium, B. cereus, B. thuringiensis, B. subtilis, and Lysinibacillus fusiformis based on 16S rRNA analysis. The calcium carbonate polymorphs produced by various bacterial isolates were analyzed by scanning electron microscopy, confocal laser scanning microscopy, X ray diffraction, and Fourier transmission infra red spectroscopy. A strainspecific precipitation of calcium carbonate forms was observed from different bacterial isolates. Based on the type of polymorph precipitated, the technology of MICCP can be applied for remediation of various building materials.

Keywords

Bacillus, calcite, vaterite, biofilm, urease, carbonic anhydrase

References

  1. Achal, V., A. Mukherjee, P. C. Basu, and M. S. Reddy. 2009. Strain improvement of Sporosarcina pasteurii for enhanced urease and calcite production. J. Ind. Microbiol. Biotechnol. 36:981-988.
    Pubmed CrossRef
  2. Bäuerlein, E. 2003. Biomineralization of unicellular organisms:An unusual membrane biochemistry for the production of inorganic nano- and microstructures. Angew. Chem. Int. 42:614-641.
    Pubmed CrossRef
  3. Braissant, O., G. Cailleau, C. Dupraz, and E. P. Verrecchia. 2003. Bacterially induced mineralization of calcium carbonate in terrestrial environments: The role of exopolysaccharides and amino acid. J. Sed. Res. 72: 485-490.
    CrossRef
  4. Castanier, S., G. Le Metayer-Levrel, and J. P. Perthuisot. 1999. Ca-carbonates precipitation and limestone genesis - the microbiogeologist point of view. Sediment. Geol. 126: 9-23.
    CrossRef
  5. Castanier, S., G. Le Métayer-Levrel, and J. P. Perthuisot. 2000. Bacterial roles in the precipitation of carbonate minerals, pp. 32-39. In R. E. Riding and S. M. Awramik (eds.). Microbial Sediments. Springer-Verlag, Heidelberg.
  6. De Yoreo, J. J. and P. M. Dove. 2004. Shaping crystals with biomolecules. Science 306: 1301-1302.
    Pubmed CrossRef
  7. Dhami, N. K., A. Mukherjee, and M. S. Reddy. 2012. Improvement in strength properties of ash bricks by bacterial calcite. Ecol. Eng. 39: 31-35.
    CrossRef
  8. Dhami, N. K., A. Mukherjee, and M. S. Reddy. 2012. Biofilm and Microbial Applications in Biomineralized concrete, pp. 137-164. In Jong Seto (ed.). Advanced Topics in Biomineralization. InTech.
  9. Ercole, C., P. Bozzelli, F. Altieri, P. Cacchio, and M. D. Gallo. 2012. Calcium carbonate mineralization: involvement of extracellular polymeric materials isolated from calcifying bacteria. Microsc. Microanal. 18: 829-839.
    Pubmed CrossRef
  10. Ercole, C., P. Cacchio, A. L. Botta, V. Centi, and A. Lepidi. 2007. Bacterially induced mineralization of calcium carbonate:The role of exopolysaccharides and capsular polysaccharides. Microsc. Microanal. 13: 42-50.
    Pubmed CrossRef
  11. Friedman, L. E., B. N. de Passerini Rossi, M. T. Messina, and M. A. Franco. 2001. Phenotype evaluation of Bordetella bronchiseptica cultures by urease activity and Congo red affinity. Lett. Appl. Microbiol. 33: 285-290.
    Pubmed CrossRef
  12. Hammes, F., N. Boon, J. De Villiers, W. Verstraete, and S. D. Siciliano. 2003. Strain-specific ureolytic microbial calcium carbonate precipitation. Appl. Environ. Microbiol. 69: 49014909.
    PMC CrossRef
  13. Holt, J. G., N. R. Krieg, P. H. A Sneath, J. T. Staley, and S. T. Williams. 1994. Bergey’s Manual of Determinative Bacteriology, 9th Ed. Williams and Wilkins, Baltimore.
  14. Karn, K. S., S. K. Chakrabarty, and M. S. Reddy. 2010. Characterization of pentachlorophenol degrading Bacillus strains from secondary pulp and paper industry sludge. Int. Biodeter. Biodegrad. 64: 609-613.
    CrossRef
  15. Kawaguchi, T. and A. W. Decho. 2002. A laboratory investigation of cyanobacterial extracellular polymeric secretion (EPS) in influencing CaCO3 polymorphism. J. Cryst. Growth 240: 230-235.
    CrossRef
  16. Lian, B., Q. Hu, J. Chen, J. Ji, and H. H. Teng. 2006. Carbonate biomineralization by soil bacterium Bacillus megaterium. Geochim. Cosmochim. Acta 70: 5522-5535.
    CrossRef
  17. Mann, S. 2001. Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry. Oxford University Press, Oxford.
  18. Meldrum, F. and H. Cölfen. 2008. Controlling mineral morphologies and structures in biological and synthetic systems. Chem. Rev. 108: 4332-4432.
    Pubmed CrossRef
  19. Merz-Preiss, M. and R. Riding. 1999. Cyanobacterial tufa calcification in two freshwater streams: Ambient environment, chemical thresholds and biological processes. Sediment Geol. 126: 103-124.
    CrossRef
  20. Mitchell, A. C., K. Dideriksen, L. H. Spangler, A. B. Cunningham, and R. Gerlach. 2010. Microbially enhanced carbon capture and storage by mineral-trapping and solubility-trapping. Environ. Sci. Technol. 44: 5270-5276.
    Pubmed CrossRef
  21. Morikawa, M., S. Kagihiro, M. Haruki, K. Takano, S. Branda, R. Kotler, and S. Kanaya. 2006. Biofilm formation by a Bacillus subtilis strain that produces polyglutamate. Microbiology 152:2801-2807.
    Pubmed CrossRef
  22. Park, I. S. and R. P. Hausinger. 1995. Requirement of carbon dioxide for in vitro assembly of urease nickel metallocenter. Science 267: 1156-1158.
    Pubmed CrossRef
  23. Qian, C., R. Wang, L. Cheng, and J. Wang. 2010. Theory of microbial carbonate precipitation and its application in restoration of cement-based materials defects. Chin. J. Chem. 28: 847-857.
    CrossRef
  24. Rivadeneyra, M. A., G., Delgado, A. Ramos-Cormenzana, and R. Delgado. 1998. Biomineralization of carbonates by Halomonas eurihalina in solid and liquid media with different salinities:Crystal formation sequence. Res. Microbiol. 149: 277-287.
    CrossRef
  25. Rodriguez-Navarro, C., C. Jimenez-Lopez, A. Rodriguez-Navarro, M. T Gonzalez-Muñoz, and M. Rodríguez-Gallego. 2007. Bacterially mediated mineralization of vaterite. Geochim. Cosmochim. Acta 71: 1197-1213.
    CrossRef
  26. Smith, K. S. and J. G. Ferry. 1999. A plant type (L class) carbonic anhydrase from the thermophilic methanoarchaeon Methanobacteium thermoautotrophicum. J. Bacteriol. 181: 6247 -6253.
    Pubmed PMC
  27. Sondi, I. and E. Matijevic. 2001. Homogeneous precipitation of calcium carbonates by enzyme catalyzed reaction. J. Colloid Interface Sci. 238: 208-214.
    Pubmed CrossRef
  28. Stahler, M. F., L. Ganter, L. Katherin, K. Manfred, and B. Stephen. 2005. Mutational analysis of Helicobacter pylori carbonic anhydrases. FEMS Immunol. Med. Microbiol. 44:183-189.
    Pubmed CrossRef
  29. Stocks-Fischer, S., J. K. Galinat, and S. S. Bang. 1999. Microbiological precipitation of CaCO3. Soil Biol. Biochem. 31:1563-1571.
    CrossRef
  30. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
    Pubmed PMC CrossRef
  31. Tourney, J. and B. T. Ngwenya. 2009. Bacterial extracellular polymeric substances (EPS) mediate CaCO3 morphology and polymorph. Chem. Geol. 262: 138-146.
    CrossRef
  32. Tsuneda, S., J. Jung, H. Hayashi, H. Aikawa, A. Hirata, and H. Sasaki. 2003. Influence of extracellular polymers on electrokinetic properties of heterotrophic bacterial cells examined by soft particle electrophoresis theory. Colloids Surf. B 29: 181-188.
    CrossRef
  33. Warren, L. A., P. A. Maurice, N. Parmar, and F. G. Ferris. 2001. Microbially mediated calcium carbonate precipitation: Implications for interpreting calcite precipitation and for solid-phase capture of inorganic contaminants. Geomicrobiol. J. 18: 93-115.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2013; 23(5): 707-714

Published online May 25, 2013 https://doi.org/10.4014/jmb.1212.11087

Copyright © The Korean Society for Microbiology and Biotechnology.

Biomineralization of Calcium Carbonate Polymorphs by the Bacterial Strains Isolated from Calcareous Sites

Navdeep Kaur Dhami 1, M. Sudhakara Reddy 1* and Abhijit Mukherjee 2

1Department of Biotechnology, Thapar University, Patiala 147004, India, 2Department of Civil Engineering, Thapar University, Patiala 147004, India

Received: December 3, 2012; Accepted: December 30, 2012

Abstract

Microbially induced calcium carbonate precipitation
(MICCP) is a naturally occurring biological process that
has various applications in remediation and restoration of
a range of building materials. In the present investigation,
five ureolytic bacterial isolates capable of inducing
calcium carbonate precipitation were isolated from
calcareous soils on the basis of production of urease,
carbonic anhydrase, extrapolymeric substances, and biofilm.
Bacterial isolates were identified as Bacillus megaterium,
B. cereus, B. thuringiensis, B. subtilis, and Lysinibacillus
fusiformis based on 16S rRNA analysis. The calcium
carbonate polymorphs produced by various bacterial
isolates were analyzed by scanning electron microscopy,
confocal laser scanning microscopy, X ray diffraction, and
Fourier transmission infra red spectroscopy. A strainspecific
precipitation of calcium carbonate forms was
observed from different bacterial isolates. Based on the
type of polymorph precipitated, the technology of MICCP
can be applied for remediation of various building materials.

Keywords: Bacillus, calcite, vaterite, biofilm, urease, carbonic anhydrase

References

  1. Achal, V., A. Mukherjee, P. C. Basu, and M. S. Reddy. 2009. Strain improvement of Sporosarcina pasteurii for enhanced urease and calcite production. J. Ind. Microbiol. Biotechnol. 36:981-988.
    Pubmed CrossRef
  2. Bäuerlein, E. 2003. Biomineralization of unicellular organisms:An unusual membrane biochemistry for the production of inorganic nano- and microstructures. Angew. Chem. Int. 42:614-641.
    Pubmed CrossRef
  3. Braissant, O., G. Cailleau, C. Dupraz, and E. P. Verrecchia. 2003. Bacterially induced mineralization of calcium carbonate in terrestrial environments: The role of exopolysaccharides and amino acid. J. Sed. Res. 72: 485-490.
    CrossRef
  4. Castanier, S., G. Le Metayer-Levrel, and J. P. Perthuisot. 1999. Ca-carbonates precipitation and limestone genesis - the microbiogeologist point of view. Sediment. Geol. 126: 9-23.
    CrossRef
  5. Castanier, S., G. Le Métayer-Levrel, and J. P. Perthuisot. 2000. Bacterial roles in the precipitation of carbonate minerals, pp. 32-39. In R. E. Riding and S. M. Awramik (eds.). Microbial Sediments. Springer-Verlag, Heidelberg.
  6. De Yoreo, J. J. and P. M. Dove. 2004. Shaping crystals with biomolecules. Science 306: 1301-1302.
    Pubmed CrossRef
  7. Dhami, N. K., A. Mukherjee, and M. S. Reddy. 2012. Improvement in strength properties of ash bricks by bacterial calcite. Ecol. Eng. 39: 31-35.
    CrossRef
  8. Dhami, N. K., A. Mukherjee, and M. S. Reddy. 2012. Biofilm and Microbial Applications in Biomineralized concrete, pp. 137-164. In Jong Seto (ed.). Advanced Topics in Biomineralization. InTech.
  9. Ercole, C., P. Bozzelli, F. Altieri, P. Cacchio, and M. D. Gallo. 2012. Calcium carbonate mineralization: involvement of extracellular polymeric materials isolated from calcifying bacteria. Microsc. Microanal. 18: 829-839.
    Pubmed CrossRef
  10. Ercole, C., P. Cacchio, A. L. Botta, V. Centi, and A. Lepidi. 2007. Bacterially induced mineralization of calcium carbonate:The role of exopolysaccharides and capsular polysaccharides. Microsc. Microanal. 13: 42-50.
    Pubmed CrossRef
  11. Friedman, L. E., B. N. de Passerini Rossi, M. T. Messina, and M. A. Franco. 2001. Phenotype evaluation of Bordetella bronchiseptica cultures by urease activity and Congo red affinity. Lett. Appl. Microbiol. 33: 285-290.
    Pubmed CrossRef
  12. Hammes, F., N. Boon, J. De Villiers, W. Verstraete, and S. D. Siciliano. 2003. Strain-specific ureolytic microbial calcium carbonate precipitation. Appl. Environ. Microbiol. 69: 49014909.
    KoreaMed CrossRef
  13. Holt, J. G., N. R. Krieg, P. H. A Sneath, J. T. Staley, and S. T. Williams. 1994. Bergey’s Manual of Determinative Bacteriology, 9th Ed. Williams and Wilkins, Baltimore.
  14. Karn, K. S., S. K. Chakrabarty, and M. S. Reddy. 2010. Characterization of pentachlorophenol degrading Bacillus strains from secondary pulp and paper industry sludge. Int. Biodeter. Biodegrad. 64: 609-613.
    CrossRef
  15. Kawaguchi, T. and A. W. Decho. 2002. A laboratory investigation of cyanobacterial extracellular polymeric secretion (EPS) in influencing CaCO3 polymorphism. J. Cryst. Growth 240: 230-235.
    CrossRef
  16. Lian, B., Q. Hu, J. Chen, J. Ji, and H. H. Teng. 2006. Carbonate biomineralization by soil bacterium Bacillus megaterium. Geochim. Cosmochim. Acta 70: 5522-5535.
    CrossRef
  17. Mann, S. 2001. Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry. Oxford University Press, Oxford.
  18. Meldrum, F. and H. Cölfen. 2008. Controlling mineral morphologies and structures in biological and synthetic systems. Chem. Rev. 108: 4332-4432.
    Pubmed CrossRef
  19. Merz-Preiss, M. and R. Riding. 1999. Cyanobacterial tufa calcification in two freshwater streams: Ambient environment, chemical thresholds and biological processes. Sediment Geol. 126: 103-124.
    CrossRef
  20. Mitchell, A. C., K. Dideriksen, L. H. Spangler, A. B. Cunningham, and R. Gerlach. 2010. Microbially enhanced carbon capture and storage by mineral-trapping and solubility-trapping. Environ. Sci. Technol. 44: 5270-5276.
    Pubmed CrossRef
  21. Morikawa, M., S. Kagihiro, M. Haruki, K. Takano, S. Branda, R. Kotler, and S. Kanaya. 2006. Biofilm formation by a Bacillus subtilis strain that produces polyglutamate. Microbiology 152:2801-2807.
    Pubmed CrossRef
  22. Park, I. S. and R. P. Hausinger. 1995. Requirement of carbon dioxide for in vitro assembly of urease nickel metallocenter. Science 267: 1156-1158.
    Pubmed CrossRef
  23. Qian, C., R. Wang, L. Cheng, and J. Wang. 2010. Theory of microbial carbonate precipitation and its application in restoration of cement-based materials defects. Chin. J. Chem. 28: 847-857.
    CrossRef
  24. Rivadeneyra, M. A., G., Delgado, A. Ramos-Cormenzana, and R. Delgado. 1998. Biomineralization of carbonates by Halomonas eurihalina in solid and liquid media with different salinities:Crystal formation sequence. Res. Microbiol. 149: 277-287.
    CrossRef
  25. Rodriguez-Navarro, C., C. Jimenez-Lopez, A. Rodriguez-Navarro, M. T Gonzalez-Muñoz, and M. Rodríguez-Gallego. 2007. Bacterially mediated mineralization of vaterite. Geochim. Cosmochim. Acta 71: 1197-1213.
    CrossRef
  26. Smith, K. S. and J. G. Ferry. 1999. A plant type (L class) carbonic anhydrase from the thermophilic methanoarchaeon Methanobacteium thermoautotrophicum. J. Bacteriol. 181: 6247 -6253.
    Pubmed KoreaMed
  27. Sondi, I. and E. Matijevic. 2001. Homogeneous precipitation of calcium carbonates by enzyme catalyzed reaction. J. Colloid Interface Sci. 238: 208-214.
    Pubmed CrossRef
  28. Stahler, M. F., L. Ganter, L. Katherin, K. Manfred, and B. Stephen. 2005. Mutational analysis of Helicobacter pylori carbonic anhydrases. FEMS Immunol. Med. Microbiol. 44:183-189.
    Pubmed CrossRef
  29. Stocks-Fischer, S., J. K. Galinat, and S. S. Bang. 1999. Microbiological precipitation of CaCO3. Soil Biol. Biochem. 31:1563-1571.
    CrossRef
  30. Tamura, K., D. Peterson, N. Peterson, G. Stecher, M. Nei, and S. Kumar. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28: 2731-2739.
    Pubmed KoreaMed CrossRef
  31. Tourney, J. and B. T. Ngwenya. 2009. Bacterial extracellular polymeric substances (EPS) mediate CaCO3 morphology and polymorph. Chem. Geol. 262: 138-146.
    CrossRef
  32. Tsuneda, S., J. Jung, H. Hayashi, H. Aikawa, A. Hirata, and H. Sasaki. 2003. Influence of extracellular polymers on electrokinetic properties of heterotrophic bacterial cells examined by soft particle electrophoresis theory. Colloids Surf. B 29: 181-188.
    CrossRef
  33. Warren, L. A., P. A. Maurice, N. Parmar, and F. G. Ferris. 2001. Microbially mediated calcium carbonate precipitation: Implications for interpreting calcite precipitation and for solid-phase capture of inorganic contaminants. Geomicrobiol. J. 18: 93-115.
    CrossRef