Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

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

  • Dhami, Navdeep Kaur (Department of Biotechnology, Thapar University) ;
  • Reddy, M. Sudhakara (Department of Biotechnology, Thapar University) ;
  • Mukherjee, Abhijit (Department of Civil Engineering, Thapar University)
  • Received : 2012.12.03
  • Accepted : 2012.12.30
  • Published : 2013.05.28
Download PDF
⟨ Previous Next ⟩

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 strain-specific 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

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. https://doi.org/10.1007/s10295-009-0578-z
  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. https://doi.org/10.1002/anie.200390176
  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.
  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. https://doi.org/10.1016/S0037-0738(99)00028-7
  5. Castanier, S., G. Le Metayer-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. https://doi.org/10.1126/science.1100889
  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. https://doi.org/10.1016/j.ecoleng.2011.11.011
  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. https://doi.org/10.1017/S1431927612000426
  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. https://doi.org/10.1017/S1431927607070122
  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. https://doi.org/10.1046/j.1472-765X.2001.00997.x
  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: 4901-4909. https://doi.org/10.1128/AEM.69.8.4901-4909.2003
  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. https://doi.org/10.1016/j.ibiod.2010.05.017
  15. Kawaguchi, T. and A. W. Decho. 2002. A laboratory investigation of cyanobacterial extracellular polymeric secretion (EPS) in influencing $CaCO_3$ polymorphism. J. Cryst. Growth 240: 230-235. https://doi.org/10.1016/S0022-0248(02)00918-1
  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. https://doi.org/10.1016/j.gca.2006.08.044
  17. Mann, S. 2001. Biomineralization: Principles and Concepts in Bioinorganic Materials Chemistry. Oxford University Press, Oxford.
  18. Meldrum, F. and H. Colfen. 2008. Controlling mineral morphologies and structures in biological and synthetic systems. Chem. Rev. 108: 4332-4432. https://doi.org/10.1021/cr8002856
  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. https://doi.org/10.1016/S0037-0738(99)00035-4
  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. https://doi.org/10.1021/es903270w
  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. https://doi.org/10.1099/mic.0.29060-0
  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. https://doi.org/10.1126/science.7855593
  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. https://doi.org/10.1002/cjoc.201090156
  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. https://doi.org/10.1016/S0923-2508(98)80303-3
  25. Rodriguez-Navarro, C., C. Jimenez-Lopez, A. Rodriguez-Navarro, M. T Gonzalez-Munoz, and M. Rodriguez-Gallego. 2007. Bacterially mediated mineralization of vaterite. Geochim. Cosmochim. Acta 71: 1197-1213. https://doi.org/10.1016/j.gca.2006.11.031
  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.
  27. Sondi, I. and E. Matijevic. 2001. Homogeneous precipitation of calcium carbonates by enzyme catalyzed reaction. J. Colloid Interface Sci. 238: 208-214. https://doi.org/10.1006/jcis.2001.7516
  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. https://doi.org/10.1016/j.femsim.2004.10.021
  29. Stocks-Fischer, S., J. K. Galinat, and S. S. Bang. 1999. Microbiological precipitation of $CaCO_3$. Soil Biol. Biochem. 31: 1563-1571. https://doi.org/10.1016/S0038-0717(99)00082-6
  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. https://doi.org/10.1093/molbev/msr121
  31. Tourney, J. and B. T. Ngwenya. 2009. Bacterial extracellular polymeric substances (EPS) mediate $CaCO_3$ morphology and polymorph. Chem. Geol. 262: 138-146. https://doi.org/10.1016/j.chemgeo.2009.01.006
  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. https://doi.org/10.1016/S0927-7765(02)00188-1
  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. https://doi.org/10.1080/01490450151079833

Cited by

  1. Biomineralization of calcium carbonates and their engineered applications: a review vol.4, pp.None, 2013, https://doi.org/10.3389/fmicb.2013.00314
  2. Bacillus megaterium mediated mineralization of calcium carbonate as biogenic surface treatment of green building materials vol.29, pp.12, 2013, https://doi.org/10.1007/s11274-013-1408-z
  3. Viability of calcifying bacterial formulations in fly ash for applications in building materials vol.40, pp.12, 2013, https://doi.org/10.1007/s10295-013-1338-7
  4. Synergistic Role of Bacterial Urease and Carbonic Anhydrase in Carbonate Mineralization vol.172, pp.5, 2013, https://doi.org/10.1007/s12010-013-0694-0
  5. A mineralogical characterization of biogenic calcium carbonates precipitated by heterotrophic bacteria isolated from cryophilic polar regions vol.12, pp.6, 2014, https://doi.org/10.1111/gbi.12102
  6. Isolation and identification of Pseudomonas azotoformans for induced calcite precipitation vol.31, pp.12, 2013, https://doi.org/10.1007/s11274-015-1948-5
  7. Metagenomic Analysis Suggests Modern Freshwater Microbialites Harbor a Distinct Core Microbial Community vol.6, pp.None, 2013, https://doi.org/10.3389/fmicb.2015.01531
  8. Influence of Exopolymeric Materials on Bacterially Induced Mineralization of Carbonates vol.175, pp.7, 2013, https://doi.org/10.1007/s12010-015-1524-3
  9. Bacillus cereus in personal care products: risk to consumers vol.37, pp.2, 2015, https://doi.org/10.1111/ics.12191
  10. Biocalcification by halophilic bacteria for remediation of concrete structures in marine environment vol.43, pp.11, 2013, https://doi.org/10.1007/s10295-016-1835-6
  11. Soil Bioconsolidation Through Microbially Induced Calcite Precipitation by Lysinibacillus sphaericus WJ-8 vol.33, pp.6, 2013, https://doi.org/10.1080/01490451.2015.1053581
  12. Calcium Carbonate Precipitation by Bacillus and Sporosarcina Strains Isolated from Concrete and Analysis of the Bacterial Community of Concrete vol.26, pp.3, 2013, https://doi.org/10.4014/jmb.1511.11008
  13. Potential use of carbonatogenic bacteria in monuments biorestoration vol.33, pp.3, 2013, https://doi.org/10.1016/j.nbt.2015.10.046
  14. Applicability of bacterial biocementation in sustainable construction materials vol.11, pp.5, 2016, https://doi.org/10.1002/apj.2014
  15. Formations of calcium carbonate minerals by bacteria and its multiple applications vol.5, pp.1, 2013, https://doi.org/10.1186/s40064-016-1869-2
  16. Isolation of Leclercia adcarboxglata Strain JLS1 from Dolostone Sample and Characterization of its Induced Struvite Minerals vol.34, pp.6, 2017, https://doi.org/10.1080/01490451.2016.1222469
  17. Diversity and Biomineralization Potential of the Epilithic Bacterial Communities Inhabiting the Oldest Public Stone Monument of Cluj-Napoca (Transylvania, Romania) vol.8, pp.None, 2013, https://doi.org/10.3389/fmicb.2017.00372
  18. Bacterial Community Dynamics and Biocement Formation during Stimulation and Augmentation: Implications for Soil Consolidation vol.8, pp.None, 2013, https://doi.org/10.3389/fmicb.2017.01267
  19. The influence of human exploration on the microbial community structure and ammonia oxidizing potential of the Su Bentu limestone cave in Sardinia, Italy vol.12, pp.7, 2013, https://doi.org/10.1371/journal.pone.0180700
  20. Application of microbially induced calcium carbonate precipitation in designing bio self-healing concrete vol.34, pp.11, 2018, https://doi.org/10.1007/s11274-018-2552-2
  21. Calcite-forming Bacillus licheniformis Thriving on Underwater Speleothems of a Hydrothermal Cave vol.35, pp.9, 2013, https://doi.org/10.1080/01490451.2018.1476626
  22. Microbial Diversity and Mineralogical-Mechanical Properties of Calcitic Cave Speleothems in Natural and in Vitro Biomineralization Conditions vol.9, pp.None, 2013, https://doi.org/10.3389/fmicb.2018.00040
  23. Novel Mechanism for Surface Layer Shedding and Regenerating in Bacteria Exposed to Metal-Contaminated Conditions vol.9, pp.None, 2013, https://doi.org/10.3389/fmicb.2018.03210
  24. A Low-Tech Bioreactor System for the Enrichment and Production of Ureolytic Microbes vol.67, pp.1, 2013, https://doi.org/10.5604/01.3001.0011.6144
  25. An XRPD and EPR spectroscopy study of microcrystalline calcite bioprecipitated by Bacillus subtilis vol.45, pp.10, 2013, https://doi.org/10.1007/s00269-018-0974-x
  26. Calcite precipitation induced by Bacillus cereus MRR2 cultured at different Ca2+ concentrations: Further insights into biotic and abiotic calcite vol.500, pp.None, 2013, https://doi.org/10.1016/j.chemgeo.2018.09.018
  27. Factors affecting the bio-cementing process of coarse sand vol.172, pp.1, 2019, https://doi.org/10.1680/jgrim.17.00039
  28. Biosequestration of heavy metals by microbially induced calcite precipitation of ureolytic bacteria vol.24, pp.1, 2013, https://doi.org/10.25083/rbl/24.1/147.153
  29. An optimum condition of MICP indigenous bacteria with contaminated wastes of heavy metal vol.21, pp.2, 2013, https://doi.org/10.1007/s10163-018-0779-5
  30. Biocalcification by Piezotolerant Bacillus sp. NIOTVJ5 Isolated from Deep Sea Sediment and its Influence on the Strength of Concrete Specimens vol.21, pp.2, 2019, https://doi.org/10.1007/s10126-018-9867-8
  31. Metal and metalloid immobilization by microbiologically induced carbonates precipitation vol.35, pp.4, 2019, https://doi.org/10.1007/s11274-019-2626-9
  32. Identification of Ureolytic Bacteria for Concrete Formation and Antifungal Activity from the Soil with Long-Term Application of Urea Fertilizer vol.252, pp.None, 2013, https://doi.org/10.1088/1755-1315/252/5/052131
  33. Factors affecting the urease activity of native ureolytic bacteria isolated from coastal areas vol.17, pp.5, 2013, https://doi.org/10.12989/gae.2019.17.5.421
  34. Calcite formation induced by Ensifer adhaerens, Microbacterium testaceum, Paeniglutamicibacter kerguelensis, Pseudomonas protegens and Rheinheimera texasensis vol.112, pp.5, 2013, https://doi.org/10.1007/s10482-018-1204-8
  35. Controlling the Distribution of Microbially Precipitated Calcium Carbonate in Radial Flow Environments vol.53, pp.10, 2013, https://doi.org/10.1021/acs.est.8b06876
  36. Microbially induced calcium carbonate precipitation: a widespread phenomenon in the biological world vol.103, pp.12, 2013, https://doi.org/10.1007/s00253-019-09861-5
  37. Unconfined Compressive Strength and Visualization of the Microstructure of Coarse Sand Subjected to Different Biocementation Levels vol.145, pp.8, 2013, https://doi.org/10.1061/(asce)gt.1943-5606.0002066
  38. Effect of Calcium Organic Additives on the Self-Healing of Concrete Microcracks in the Presence of a New Isolate Bacillus sp. BY1 vol.31, pp.10, 2013, https://doi.org/10.1061/(asce)mt.1943-5533.0002711
  39. Effects of different calcium sources on the mineralization and sand curing of CaCO3 by carbonic anhydrase-producing bacteria vol.9, pp.70, 2013, https://doi.org/10.1039/c9ra09025h
  40. Factors affecting the performance of microbial-induced carbonate precipitation (MICP) treated soil: a review vol.79, pp.5, 2020, https://doi.org/10.1007/s12665-020-8840-9
  41. Analysis and optimization of process parameters for in vitro biomineralization of CaCO3 by Klebsiella pneumoniae, isolated from a stalactite from the Sahastradhara cave vol.10, pp.14, 2020, https://doi.org/10.1039/d0ra00090f
  42. Removal of Heavy Metals Zinc, Lead, and Cadmium by Biomineralization of Urease-Producing Bacteria Isolated from Iranian Mine Calcareous Soils vol.20, pp.1, 2013, https://doi.org/10.1007/s42729-019-00121-z
  43. Understanding and creating biocementing beachrocks via biostimulation of indigenous microbial communities vol.104, pp.8, 2013, https://doi.org/10.1007/s00253-020-10474-6
  44. Isolation and Identification of Local Bactria Produced from Soil-Borne Urease vol.901, pp.None, 2013, https://doi.org/10.1088/1757-899x/901/1/012035
  45. Carbonate and Oxalate Crystallization by Interaction of Calcite Marble with Bacillus subtilis and Bacillus subtilis-Aspergillus niger Association vol.10, pp.9, 2020, https://doi.org/10.3390/cryst10090756
  46. Scalable Chemical Synthesis Route to Manufacture pH-Responsive Janus CaCO3 Micromotors vol.36, pp.42, 2013, https://doi.org/10.1021/acs.langmuir.0c02148
  47. Microbiologically Induced Carbonate Precipitation in the Restoration and Conservation of Cultural Heritage Materials vol.25, pp.23, 2013, https://doi.org/10.3390/molecules25235499
  48. Research Progress and Application of Biomineralization vol.10, pp.4, 2013, https://doi.org/10.12677/amb.2021.104022
  49. Microbial-Induced Carbonate Precipitation: A Review on Influencing Factors and Applications vol.2021, pp.None, 2013, https://doi.org/10.1155/2021/9974027
  50. Isolation, identification and growth conditions of calcite producing bacteria from urea-rich soil vol.15, pp.1, 2013, https://doi.org/10.5897/ajmr2020.9445
  51. Gypsum Amendment Induced Rapid Pyritization in Fe-Rich Mine Tailings from Doce River Estuary after the Fundão Dam Collapse vol.11, pp.2, 2013, https://doi.org/10.3390/min11020201
  52. Ammonium monoethyloxalate (AmEtOx): a new agent for the conservation of carbonate stone substrates vol.45, pp.12, 2021, https://doi.org/10.1039/d0nj06001a
  53. Utilization of Biomineralized Steel Slag in Cement Mortar to Improve Its Properties vol.33, pp.6, 2021, https://doi.org/10.1061/(asce)mt.1943-5533.0003749
  54. Bioconservation of Historic Stone Buildings-An Updated Review vol.11, pp.12, 2013, https://doi.org/10.3390/app11125695
  55. Influence of the Grouting Parameters on Microbially Induced Carbonate Precipitation for Soil Stabilization vol.38, pp.9, 2013, https://doi.org/10.1080/01490451.2021.1946623
  56. Calcite and Vaterite Biosynthesis by Nitrate Dissimilating Bacteria in Carbonatogenesis Process under Aerobic and Anaerobic Conditions vol.38, pp.9, 2021, https://doi.org/10.1080/01490451.2021.1951398
  57. Profiling of Bacteria Capable of Precipitating CaCO3 on the Speleothem Surfaces in Dupnisa Cave, Kırklareli, Turkey vol.38, pp.9, 2013, https://doi.org/10.1080/01490451.2021.1964110
  58. Improving the Strength and Leaching Characteristics of Pb-Contaminated Silt through MICP vol.11, pp.11, 2013, https://doi.org/10.3390/cryst11111303
  59. Bio-composites treatment for mitigation of current-induced riverbank soil erosion vol.800, pp.None, 2013, https://doi.org/10.1016/j.scitotenv.2021.149513
  60. Investigation on the Impact of Cementation Media Concentration on Properties of Biocement under Stimulation and Augmentation Approaches vol.26, pp.1, 2013, https://doi.org/10.1061/(asce)hz.2153-5515.0000662
  61. Microbial Depolymerization of Epoxy Resins: A Novel Approach to a Complex Challenge vol.12, pp.1, 2013, https://doi.org/10.3390/app12010466