Skip to main content
Log in

Non-ureolytic calcium carbonate precipitation by Lysinibacillus sp. YS11 isolated from the rhizosphere of Miscanthus sacchariflorus

  • Microbial Ecology and Environmental Microbiology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

Although microbially induced calcium carbonate precipitation (MICP) through ureolysis has been widely studied in environmental engineering fields, urea utilization might cause environmental problems as a result of ammonia and nitrate production. In this study, many non-ureolytic calcium carbonate-precipitating bacteria that induced an alkaline environment were isolated from the rhizosphere of Miscanthus sacchariflorus near an artificial stream and their ability to precipitate calcium carbonate minerals with the absence of urea was investigated. MICP was observed using a phase-contrast microscope and ion-selective electrode. Only Lysinibacillus sp. YS11 showed MICP in aerobic conditions. Energy dispersive X-ray spectrometry and X-ray diffraction confirmed the presence of calcium carbonate. Field emission scanning electron microscopy analysis indicated the formation of morphologically distinct minerals around cells under these conditions. Monitoring of bacterial growth, pH changes, and Ca2+ concentrations under aerobic, hypoxia, and anaerobic conditions suggested that strain YS11 could induce alkaline conditions up to a pH of 8.9 and utilize 95% of free Ca2+ only under aerobic conditions. Unusual Ca2+ binding and its release from cells were observed under hypoxia conditions. Biofilm and extracellular polymeric substances (EPS) formation were enhanced during MICP. Strain YS11 has resistance at high pH and in high salt concentrations, as well as its spore-forming ability, which supports its potential application for self-healing concrete.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahmed, I., Yokota, A., Yamazoe, A., and Fujiwara, T. 2007. Proposal of Lysinibacillus boronitolerans gen. nov. sp. nov., and transfer of Bacillus fusiformis to Lysinibacillus fusiformis comb. nov. and Bacillus sphaericus to Lysinibacillus sphaericus comb. nov. Int. J. Syst. Evol. Microbiol. 57, 1117–1125.

    Article  CAS  PubMed  Google Scholar 

  • Atlas, R.M. 2005. Mineral salts agar, In Handbook of Media for Environmental Microbiology. 2nd ed. CRC Press, Taylor and Francis, New York, USA.

    Google Scholar 

  • Barabesi, C., Galizzi, A., Mastromei, G., Rossi, M., Tamburini, E., and Perito, B. 2007. Bacillus subtilis gene cluster involved in calcium carbonate biomineralization. J. Bacteriol. 189, 228–235.

    Article  CAS  PubMed  Google Scholar 

  • Boquet, E., Boronat, A., and Ramos-Cormenzana, A. 1973. Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246, 527–529.

    Article  Google Scholar 

  • Braissant, O., Cailleau, G., Dupraz, C., and Verrecchia, E.P. 2003. Bacterially induced mineralization of calcium carbonate in terrestrial environments: the role of exopolysaccharides and amino acids. J. Sedimentary Res. 73, 485–490.

    Article  CAS  Google Scholar 

  • Braissant, O., Decho, A.W., Dupraz, C., Glunk, C., Przekop, K.M., and Visscher, P.T. 2007. Exopolymeric substances of sulfate-reducing bacteria: interactions with calcium at alkaline pH and implication for formation of carbonate minerals. Geobiology 5, 401–411.

    Article  CAS  Google Scholar 

  • Dhami, N.K., Reddy, M.S., and Mukherjee, A. 2013. Biomineralization of calcium carbonates and their engineered applications: a review. Front. Microbiol. 4, 314.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dupraz, C., Reid, R.P., Braissant, O., Decho, A.W., Norman, R.S., and Visscher, P.T. 2009. Processes of carbonate precipitation in modern microbial mats. Earth Sci. Rev. 96, 141–162.

    Article  CAS  Google Scholar 

  • Dupraz, C., Visscher, P.T., Baumgartner, L.K., and Reid, R.P. 2004. Microbe-mineral interactions: early carbonate precipitation in a hypersaline lake (Eleuthera Island, Bahamas). Sedimentology 51, 745–765.

    Article  CAS  Google Scholar 

  • Ehrlich, H.L. 2002. Geomicrobiology. 4th ed. Taylor and Francis, New York, USA.

    Google Scholar 

  • Ercole, C., Cacchio, P., Botta, A.L., Centi, V., and Lepidi, A. 2007. Bacterially induced mineralization of calcium carbonate: the role of exopolysaccharides and capsular polysaccharides. Microsc. Microanal. 13, 42–50.

    Article  CAS  PubMed  Google Scholar 

  • Falkowski, P.G., Fenchel, T., and Delong, E.F. 2008. The microbial engines that drive earth’s biogeochemical cycles. Science 320, 1034–1039.

    Article  CAS  PubMed  Google Scholar 

  • Farhangi, M.B., Safari Sinegani, A.A., Mosaddeghi, M.R., Unc, A., and Khodakaramian, G. 2013. Impact of calcium carbonate and temperature on survival of Escherichia coli in soil. J. Environ. Manage. 119, 13–19.

    Article  CAS  PubMed  Google Scholar 

  • Ferris, F.G., Stehmeier, L.G., Kantzas, A., and Mourits, F.M. 1997. Bacteriogenic mineral plugging. J. Can. Pet. Technol. 36, 56–61.

    Article  Google Scholar 

  • Fujita, Y., Ferris, F.G., Lawson, R.D., Colwell, F.S., and Smith, R.W. 2000. Calcium carbonate precipitation by ureolytic subsurface bacteria. Geomicrobiol. J. 17, 305–318.

    Article  CAS  Google Scholar 

  • Gadd, G.M. 2010. Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156, 609–643.

    Article  CAS  PubMed  Google Scholar 

  • Hamdan, N., Edward K.J., Rittmann, B.E., and Karatas, I. 2011. Carbonate mineral precipitation for soil improvement through microbial denitrification. Geo-Frontiers Congress 2011, 3925–3934.

    Google Scholar 

  • Hammes, F., Boon, N., De Villiers, J., Verstraete, W., and Siciliano, S.D. 2003. Strain-specific ureolytic microbial calcium carbonate precipitation. Appl. Environ. Microbiol. 69, 4901–4909.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hammes, F. and Verstraete, W. 2002. Key roles of pH and calcium metabolism in microbial carbonate precipitation. Rev. Environ. Sci. Biotechnol. 1, 3–7.

    Article  CAS  Google Scholar 

  • Hazen, R.M., Papineau, D., Bleeker, W., Downs R.T., Ferry, J.M., McCoy, T.J, Sverjensky, D.A., and Yang, H. 2008. Mineral evolution. Am. Mineral. 93, 1693–1720.

    Article  CAS  Google Scholar 

  • Kim, H.J., Eom, H.J., Park, C., Jung, J., Shin, B., Kim, W., Chung, N., Choi, I.G., and Park, W. 2016a. Calcium carbonate precipitation by Bacillus and Sporosarcina strains isolated from concrete and analysis of the bacterial community of concrete. J. Microbiol. Biotechnol. 26, 540–548.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J.G., Park, S.J., Damstéc, J.S.S., Schoutenc, S., Rijpstra, W.I.C., Jung, M.Y., Kima, S.J., Gwaka, J.H., Honga, H., Sia, O.J., et al. 2016b. Hydrogen peroxide detoxification is a key mechanism for growth of ammonia-oxidizing archaea. Proc. Natl. Acad. Sci. USA 113, 7888–7893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mishra, V. 2015. Modelling of the batch biosorption system: study on exchange of protons with cell wall-bound mineral ions. Environ. Technol. 36, 3194–3200.

    Article  CAS  PubMed  Google Scholar 

  • Nolan, R.A. 1971. Amino acids and growth factors in vitamin-free casamino acids. Mycologia 63, 1231–234.

    Article  CAS  PubMed  Google Scholar 

  • Park, S.J., Park, Y.M., Chun, W.Y., Kim, W.J., and Ghim, S.Y. 2010. Calcite-forming bacteria for compressive strength improvement in mortar. J. Microbiol. Biotechnol. 20, 782–788.

    CAS  PubMed  Google Scholar 

  • Phillips, A.J., Gerlach, R., Lauchnor, E., Mitchell, A.C., Cunningham, A.B., and Spangler, L. 2013. Engineered applications of ureolytic biomineralization: a review. Biofouling 29, 715–733.

    Article  CAS  PubMed  Google Scholar 

  • Priest, F.G., Goodfellow, M., and Todd, C. 1988. A numerical classification of the genus Bacillus. J. Gen. Microbiol. 134, 1847–1882.

    CAS  PubMed  Google Scholar 

  • Reeburgh, W.S. 2007. Oceanic methane biogeochemistry. Chem. Rev. 107, 486–513.

    Article  CAS  PubMed  Google Scholar 

  • Riding, R. 2000. Microbial carbonates: the geological record of calcified bacterial-algal mats and biofilms. Sedimentology 47, 179–214.

    Article  CAS  Google Scholar 

  • Rodriguez-Navarro, C., Rodriguez-Gallego, M., Ben Chckroun, K., and Gonzalez-Munoz, M.T. 2003. Conservation of ornamental stone by Myxococcus xanthus-induced carbonate biomineralization. Appl. Environ. Microbiol. 69, 2182–2193.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seifan, M., Samani, A.K., and Berenjian, A. 2017. New insights into the role of pH and aeration in the bacterial production of calcium carbonate (CaCO3). Appl. Microbiol. Biotechnol. 101, 3131–3142.

    Article  CAS  PubMed  Google Scholar 

  • Shirakawa, M.A., Cincotto, M.A., Atencio, D., Gaylarde, C.C., and John, V.M. 2011. Effect of culture medium on biocalcification by Pseudomonas putida, Lysinibacillus sphaericus and Bacillus subtilis. Braz. J. Microbiol. 42, 499–507.

    Article  PubMed  PubMed Central  Google Scholar 

  • Silva, F.B., Boon, N., De Belie, N., and Verstraete, W. 2015. Industrial application of biological self-healing concrete: challenges and economical feasibility. J. Commer. Biotechnol. 21, 31–38.

    Article  Google Scholar 

  • Thomas, K.J. and Rice, C.V. 2014. Revised model of calcium and magnesium binding to the bacterial cell wall. Biometals 27, 1361–1370.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Paassen, L.A., Daza, C.M., Staal, M., Sorokin, D.Y., Van Der Zon, W., and Van Loosdrecht, M.C. 2010. Potential soil reinforcement by biological denitrification. Ecol. Eng. 36, 168–175.

    Article  Google Scholar 

  • Wan, S., Li, G., An, T., Guo, B., Sun, L., Zu, L., and Ren, A. 2010. Biodegradation of ethanethiol in aqueous medium by a new Lysinibacillus sphaericus strain RG-1 isolated from activated sludge. Biodegradation 21, 1057–1066.

    Article  CAS  PubMed  Google Scholar 

  • Wang, J., Ersan, Y.C., Boon, N., and Belie N.D. 2016. Application of microorganisms in concrete: a promising sustainable strategy to improve concrete durability. Appl. Microbiol. Biotechnol. 100, 2993.

    Article  CAS  PubMed  Google Scholar 

  • Warren, L.A. and Ferris, F.G. 1998. Continuum between sorption and precipitation of Fe (III) on microbial surfaces. Environ. Sci. Technol. Lett. 21, 2331–2337.

    Article  Google Scholar 

  • Warren, L.A., Maurice, P.A., Parmar, N., and Ferris, F.G. 2001. Microbially mediated calcium carbonate precipitation: implications for interpreting calcite precipitation and for solid-phase capture of inorganic contaminants. Geomicrobiol. J. 18, 93–115.

    Article  CAS  Google Scholar 

  • Zhu, T. and Dittrich, M. 2016. Carbonate precipitation through microbial activities in natural environment, and their potential in biotechnology: a review. Front. Bioeng. Biotechnol. 4, 4.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Woojun Park.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, Y.S., Kim, H.J. & Park, W. Non-ureolytic calcium carbonate precipitation by Lysinibacillus sp. YS11 isolated from the rhizosphere of Miscanthus sacchariflorus . J Microbiol. 55, 440–447 (2017). https://doi.org/10.1007/s12275-017-7086-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-017-7086-z

Keywords

Navigation