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Microbially Induced Carbonate Precipitation Techniques for the Remediation of Heavy Metal and Trace Element–Polluted Soils and Water

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Abstract

Heavy metal pollution in soil and water has been of worldwide concern due to their biotoxicity/ecotoxicity in the ecosystem, accumulation in the food chain, and persistence in the environment. Microbially induced carbonate precipitation (MICP) is known as an efficient and cost-effective biogeochemical process for the remediation of heavy metals in contaminated environment. This study reviews the mechanisms of biomineralization of urease-producing microorganisms and their biogeochemical process with various heavy metals and trace elements. Biogeochemical factors affecting the formation of carbonate biominerals were discussed. These factors included the growth and urease activity of microorganisms, calcium concentration and coexisted cations/anions, dissolved inorganic carbon, pH, redox potential, etc. In addition, the mechanisms of the biomineral morphology and its controlling factors such as medium types, microbial species, and extracellular polymeric substance were analyzed as well. Finally, the challenge and current knowledge gap on further application of MICP in remediation of heavy metal–, trace element–, and U-polluted soils and water were presented.

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References

  • Achal, V., Mukherjee, A., Basu, P. C., et al. (2009). Strain improvement of Sporosarcina pasteurii for enhanced urease and calcite production. Journal of Industrial Microbiology & Biotechnology, 36(7), 981–988.

    Article  CAS  Google Scholar 

  • Achal, V., Pan, X., & Zhang, D. (2011). Remediation of copper-contaminated soil by Kocuria flava CR1, based on microbially induced calcite precipitation. Ecological Engineering, 37(10), 1601–1605.

    Article  Google Scholar 

  • Achal, V., Pan, X., Fu, Q., et al. (2012a). Biomineralization based remediation of As(III) contaminated soil by Sporosarcina ginsengisoli. Journal of Hazardous Materials, 201, 178–184.

    Article  CAS  Google Scholar 

  • Achal, V., Pan, X., Zhang, D., & Fu, Q. (2012b). Bioremediation of Pb-contaminated soil based on microbially induced calcite precipitation. Journal of Microbiology and Biotechnology, 22(2), 244–247.

    Article  CAS  Google Scholar 

  • Achal, V., Pan, X., Lee, D. J., et al. (2013). Remediation of Cr(VI) from chromium slag by biocementation. Chemosphere, 93(7), 1352–1358.

    Article  CAS  Google Scholar 

  • Anbu, P., Kang, C. H., Shin, Y. J., & So, J. S. (2016). Formations of calcium carbonate minerals by bacteria and its multiple applications. Springerplus, 5(1), 1–26.

    Article  CAS  Google Scholar 

  • Bains, A., Dhami, N. K., Mukherjee, A., & Reddy, M. S. (2015). Influence of exopolymeric materials on bacterially induced mineralization of carbonates. Applied Biochemistry & Biotechnology, 175(7), 3531–3541.

    Article  CAS  Google Scholar 

  • Bansal, R., Dhami, N. K., Mukherjee, A., & Reddy, M. S. (2016). Biocalcification by halophilic bacteria for remediation of concrete structures in marine environment. Journal of Industrial Microbiology & Biotechnology, 43(11), 1–9.

    Article  CAS  Google Scholar 

  • Barabesi, C., Galizzi, A., Mastromei, G., Rossi, M., Tamburini, E., & Perito, B. (2007). Bacillus subtilis gene cluster involved in calcium carbonate biomineralization. Journal of Bacteriology, 189(1), 228–235.

    Article  CAS  Google Scholar 

  • Bazylinski, D. A., & Frankel, R. B. (2003). Biologically controlled mineralization in prokaryotes. Reviews in Mineralogy and Geochemistry, 54(1), 217–247.

    Article  CAS  Google Scholar 

  • Beveridge, T. J., & Fyfe, W. S. (1985). Metal fixation by bacterial cell walls. Canadian Journal of Earth Sciences, 22(12), 1893–1898.

    Article  CAS  Google Scholar 

  • Beveridge, T. J., & Murray, R. G. (1980). Sites of metal deposition in the cell wall of Bacillus subtilis. Journal of Bacteriology, 141(2), 876–887.

    Article  CAS  Google Scholar 

  • Bindschedler, S., Cailleau, G., & Verrecchia, E. (2016). Role of fungi in the biomineralization of calcite. Minerals, 6(41), 1–19.

    Google Scholar 

  • Bishop, Paul. (2000). Pollution prevention: Fundamentals and practice. McGraw-Hall.

  • Boulos, R. A., Zhang, F., Tjandra, E. S., Martin, A. D., Spagnoli, D., & Raston, C. L. (2014). Spinning up the polymorphs of calcium carbonate. Science and Reports, 4(1), 1–6.

    Google Scholar 

  • Chen, X., & Achal, V. (2019). Biostimulation of carbonate precipitation process in soil for copper immobilization. Journal of Hazardous Materials, 368, 705–713.

    Article  CAS  Google Scholar 

  • Chen, X., & Achal, V. (2020). Effect of simulated acid rain on the stability of calcium carbonate immobilized by microbial carbonate precipitation. Journal of Environmental Management, 264, 110419.

    Article  CAS  Google Scholar 

  • Chen, L., Shen, Y. H., Xie, A. J., et al. (2009). Bacteria-mediated synthesis of metal carbonate minerals with unusual morphologies and structures. Crystal Growth & Design, 9(2), 743–754.

    Article  CAS  Google Scholar 

  • Cheng, Y., & Zhao, X. Q. (2016). Study on the consolidation and mineralization of Pb2+ by carbonate-mineralization bacteria. Research of Environmental Sciences, 10, 15.

    Google Scholar 

  • Cuaxinque-Flores, G., Aguirre-Noyola, J. L., Hernández-Flores, G., Martínez-Romero, E., Romero-Ramírez, Y., & Talavera-Mendoza, O. (2020) Bioimmobilization of toxic metals by precipitation of carbonates using Sporosarcina luteola: An in vitro study and application to sulfide-bearing tailings. Science of The Total Environment, 138124.

  • Dai, Y. D., & Shen, J. Y. (1995). Minerals in biological systems. Journal of Zoology, 4, 58–61.

    Google Scholar 

  • DeJong, J. T., Martinez, B. C., Mortensen, B. M., Nelson, D. C., Waller, J. T., Weil, M. H., Ginn, T. R., Weathers, T., Barkouki, T., Fujita, Y., Redden, G., Hunt, C., Major, D., & Tunyu, B. (2009). Upscaling of bio-mediated soil improvement. Idaho National Laboratory (INL).

  • DeJong, J. T., Mortensen, B. M., Martinez, B. C., & Nelson, D. C. (2010). Bio-mediated soil improvement. Ecological Engineering, 36(2), 197–210.

    Article  Google Scholar 

  • Dhami, N. K., Reddy, M. S., & Mukherjee, A. (2013). Biomineralization of calcium carbonate polymorphs by the bacterial strains isolated from calcareous sites. Journal of Microbiology and Biotechnology, 23(5), 707–714.

    Article  CAS  Google Scholar 

  • Dhami, N. K., Mukherjee, A., & Reddy, M. S. (2016). Micrographical, minerological and nano-mechanical characterisation of microbial carbonates from urease and carbonic anhydrase producing bacteria. Ecological Engineering, 94, 443–454.

    Article  Google Scholar 

  • Dhami, N. K., Quirin, M. E. C., & Mukherjee, A. (2017). Carbonate biomineralization and heavy metal remediation by calcifying fungi isolated from karstic caves. Ecological Engineering, 103, 106–117.

    Article  Google Scholar 

  • Doi, K., Fujino, Y. (2013). Biomineralization in geothermal environments. In Thermophilic microbes in environmental and industrial biotechnology (pp. 233–247). Springer.

  • Duan, Q., Lee, J., Liu, Y., et al. (2016). Distribution of heavy metal pollution in surface soil samples in China: A graphical review. Bulletin of Environmental Contamination and Toxicology, 97(3), 303–309.

    Article  CAS  Google Scholar 

  • Dupraz, C., Reid, R. P., Braissant, O., et al. (2009). Processes of carbonate precipitation in modern microbial mats. Earth-Science Reviews, 96(3), 141–162.

    Article  CAS  Google Scholar 

  • Ferris, F. G., Beveridge, T. J., & Fyfe, W. S. (1986). Iron-silica crystallite nucleation by bacteria in a geothermal sediment. Nature, 320(6063), 609–611.

    Article  CAS  Google Scholar 

  • Ferris, F. G., Fyfe, W. S., & Beveridge, T. J. (1987). Bacteria as nucleation sites for authigenic minerals in a metal-contaminated lake sediment. Chemical Geology, 63(3–4), 225–232.

    Article  CAS  Google Scholar 

  • Frankel, R. B., & Bazylinski, D. A. (2003). Biologically induced mineralization by bacteria. Reviews in Mineralogy and Geochemistry, 54(1), 95–114.

    Article  CAS  Google Scholar 

  • Fujita, Y., Ferris, F. G., Lawson, R. D., et al. (2000). Subscribed content calcium carbonate precipitation by ureolytic subsurface bacteria. Geomicrobiology Journal, 17(4), 305–318.

    Article  CAS  Google Scholar 

  • Fujita, Y., Redden, G. D., Ingram, J. C., et al. (2004). Strontium incorporation into calcite generated by bacterial ureolysis. Geochimica Et Cosmochimica Acta, 68(15), 3261–3270.

    Article  CAS  Google Scholar 

  • Fujita, Y., Taylor, J. L., Gresham, T. L. T., et al. (2008). Stimulation of microbial urea hydrolysis in groundwater to enhance calcite precipitation. Environmental Science & Technology, 42(8), 3025–3032.

    Article  CAS  Google Scholar 

  • Gadd, G. M. (1994). Interactions of fungi with toxic Metals. In: K. A., Powell, A., Renwick, J. F., Peberdy (Eds), The Genus Aspergillus. Boston, MA.

  • Gadd, G. M. (2007). Geomycology: Biogeochemical transformations of rocks, minerals, metals and radionuclides by fungi, bioweathering and bioremediation. Mycological Research, 111(1), 3–49.

    Article  CAS  Google Scholar 

  • Gao, X. N. (2013). Current status of soil heavy metal pollution and research progress of remediation technology. Modern Agricultural Science and Technology, 9, 229–231.

    Google Scholar 

  • Gebauer, D., Gunawidjaja, P. N., Ko, J. Y., Bacsik, Z., Aziz, B., Liu, L., Hu, Y., Bergstrom, L., Tai, C. W., Sham, T. K., Eden, M., & Hedin, N. (2010). Proto-calcite and proto-vaterite in amorphous calcium carbonates. Angewandte Chemie (international Ed. in English), 49(47), 8889–8891.

    Article  CAS  Google Scholar 

  • Gorospe, C. M., Han, S. H., Kim, S. G., Park, J. Y., Kang, C. H., Jeong, J. H., & So, J. S. (2013). Effects of different calcium salts on calcium carbonate crystal formation by Sporosarcina pasteurii KCTC 3558. Biotechnology & Bioprocess Engineering, 18(5), 903–908.

    Article  CAS  Google Scholar 

  • Govarthanan, M., Lee, K. J., Cho, M., et al. (2013). Significance of autochthonous Bacillus sp. KK1 on biomineralization of lead in mine tailings. Chemosphere, 90(8), 2267–2272.

    Article  CAS  Google Scholar 

  • Guo, K., Han, F. X., Arslan, Z., McComb, J., Mao, X., Zhang, R., Sudarson, S., & Yu, H. (2015). Adsorption of Cs from water on surface modified MCM-41 mesosilicate. Water Air and Soil Pollution, 226, 288–297.

    Article  CAS  Google Scholar 

  • Guo, K., Han, F. X., Kingery, W., Sun, H., & Zhang, J. (2016). Development of novel nanomaterials for remediation of heavy metals and radionuclides in contaminated water. Nanotechnology for Environmental Engineering (Springer), 1, 7.

    Article  Google Scholar 

  • Guo, K., Larson, S. L., Ballard, J. H., Arslan, Z., Zhang, R., Ran, Y., Su, Y., & Han, F. X. (2018). Novel magnetic nanocarbon and its adsorption of Hg and Pb from water. Water Air and Soil Pollution, 229, 122.

    Article  CAS  Google Scholar 

  • Hammes, F., & Verstraete, W. (2002). Key roles of pH and calcium metabolism in microbial carbonate precipitation. Reviews in Environmental Science and Biotechnology, 1(1), 3–7.

    Article  CAS  Google Scholar 

  • Hammes, F., Boon, N., De Villiers, J., et al. (2003). Strain-specific ureolytic microbial calcium carbonate precipitation strain-specific ureolytic microbial calcium carbonate precipitation. Applied & Environmental Microbiology, 69(8), 4901–4909.

    Article  CAS  Google Scholar 

  • Han, F. X., & Singer, A. (2007). Global perspectives of anthropogenic interferences in the natural trace element distribution. In F. X. Han, Biogeochemistry of trace elements in arid environments (pp. 303–327). Springer Dordrecht.

  • Han, F. X., Banin, A., Su, Y., et al. (2002). Industrial age anthropogenic inputs of heavy metals into the pedosphere. Naturwissenschaften, 89, 497–504.

    Article  CAS  Google Scholar 

  • Han, F. X., Su, Y., Monts, D. L., Plodinec, M. J., Banin, A., & Triplett, G. B. (2003). Assessment of global industrial-age anthropogenic arsenic contamination. Naturwissenschaften, 90, 395–401.

    Article  CAS  Google Scholar 

  • Han, F. X., Sridhar, B. B. M., Monts, D. L., & Su, Y. (2004). Phytoavailability and toxicity of trivalent and hexavalent chromium to Brassica juncea. New Phytologist, 162(2), 489–499.

    Article  CAS  Google Scholar 

  • Ji, B., Chen, W., Fan, J., Song, H., & Wei, T. (2017). Research progress on microbial induced calcium precipitation by ureolytic microbes and its prospect in engineering application.Journal of Nanjing University (Natural Science Edition), 53, 191–198.

  • Jiang, N. J., Liu, R., Du, Y. J., et al. (2019). Microbial induced carbonate precipitation for immobilizing Pb contaminants: Toxic effects on bacterial activity and immobilization efficiency. Science of the Total Environment, 672, 722–731.

    Article  CAS  Google Scholar 

  • Jóźwiak, T., Filipkowska, U., Szymczyk, P., & Mielcarek, A. (2019). Sorption of nutrients (orthophosphate, nitrate III and V) in an equimolar mixture of P-PO4, N-NO2 and N-NO3 using chitosan. Arabian Journal of Chemistry, 12(8), 4104–4117.

    Article  CAS  Google Scholar 

  • Kang, C. H., Han, S. H., Shin, Y. J., Oh, S. J., & So, J. S. (2014). Bioremediation of Cd by microbially induced calcite precipitation. Applied Biochemistry and Biotechnology, 172(6), 2907–2915.

    Article  CAS  Google Scholar 

  • Kang, C. H., Oh, S. J., Shin, Y. J., et al. (2015). Bioremediation of lead by ureolytic bacteria isolated from soil at abandoned metal mines in South Korea. Ecological Engineering, 74, 402–407.

    Article  Google Scholar 

  • Kawaguchi, T., & Decho, A. W. (2002). A laboratory investigation of cyanobacterial extracellular polymeric secretions (EPS) in influencing CaCO3 polymorphism. Journal of Crystal Growth, 240(1–2), 230–235.

    Article  CAS  Google Scholar 

  • Kim, H. J., Shin, B., Lee, Y. S., & Park, W. (2017). Modulation of calcium carbonate precipitation by exopolysaccharide in Bacillus sp. JH7. Applied Microbiology & Biotechnology, 101, 6551–6561.

    Article  CAS  Google Scholar 

  • Kumari, D., Pan, X., Lee, D. J., & Achal, V. (2014). Immobilization of cadmium in soil by microbially induced carbonate precipitation with Exiguobacterium undae at low temperature. International Biodeterioration & Biodegradation, 94, 98–102.

    Article  CAS  Google Scholar 

  • Langdon, C., Takahashi, T., Sweeney, C., Chipman, D., Goddard, J., Marubini, F., Aceves, H., Barnett, H., & Atkinson, M. J. (2000). Effect of calcium carbonate saturation state on the calcification rate of an experimental coral reef. Global Biogeochemical Cycles, 14(2), 639–654.

    Article  CAS  Google Scholar 

  • Lauchnor, E. G., Schultz, L. N., Bugni, S., et al. (2013). Bacterially induced calcium carbonate precipitation and strontium coprecipitation in a porous media flow system. Environmental Science & Technology, 47(3), 1557–1564.

    Article  CAS  Google Scholar 

  • Li, M., Cheng, X., & Guo, H. (2013a). Heavy metal removal by biomineralization of urease producing bacteria isolated from soil. International Biodeterioration & Biodegradation, 76, 81–85.

    Article  CAS  Google Scholar 

  • Li, W., Chen, W. S., Zhou, P. P., et al. (2013b). Influence of initial pH on the precipitation and crystal morphology of calcium carbonate induced by microbial carbonic anhydrase. Colloids and Surfaces. b, Biointerfaces, 102, 281–287.

    Article  CAS  Google Scholar 

  • Li, Q., Csetenyi, L., Paton, G. I., & Gadd, G. M. (2015a). CaCO3 and SrCO3 bioprecipitation by fungi isolated from calcareous soil. Environmental Microbiology, 17(8), 3082–3097.

    Article  CAS  Google Scholar 

  • Li, X., Chopp, D. L., Russin, W. A., Brannon, P. T., Parsek, M. R., & Packman, A. I. (2015b). Spatial patterns of carbonate biomineralization in biofilms. Applied and Environmental Microbiology, 81(21), 7403–7410.

    Article  CAS  Google Scholar 

  • Li, Q., Zhang, B. J., Ge, Q. Y., et al. (2018). Calcium carbonate precipitation induced by calcifying bacteria in culture experiments: Influence of the medium on morphology and mineralogy. International Biodeterioration & Biodegradation, 134, 83–92.

    Article  CAS  Google Scholar 

  • Lian, B., Hu, Q. N., Chen, J., et al. (2006). Carbonate biomineralization induced by soil bacterium Bacillus megaterium. Geochimica et Cosmochimica Acta, 70(22), 5522–5535.

    Article  CAS  Google Scholar 

  • Liang, X., Hillier, S., Pendlowski, H., et al. (2015). Uranium phosphate biomineralization by fungi. Environmental Microbiology, 17(6), 2064–2075.

    Article  CAS  Google Scholar 

  • Liu, Z. H. (2001). The role of carbonic anhydrase as an activator in carbonate rock dissolution and its significance in atmospheric CO2 precipitation. Acta Geosicientia Sinica, 75, 275-278.

  • Liu, H., Ojha, B., Morris, C., et al. (2015). Positively charged chitosan and N-trimethyl chitosan inhibit Aβ40 fibrillogenesis. Biomacromolecules, 16(8), 2363–2373.

    Article  CAS  Google Scholar 

  • López-García, P., Kazmierczak, J., Benzerara, K., et al. (2005). Bacterial diversity and carbonate precipitation in the giant microbialites from the highly alkaline Lake Van Turkey. Extremophiles, 9(4), 263–274.

    Article  CAS  Google Scholar 

  • Lópezmoreno, A., Sepúlvedasánchez, J. D., Mercedes Alonso Guzmán, E. M., et al. (2014). Calcium carbonate precipitation by heterotrophic bacteria isolated from biofilms formed on deteriorated ignimbrite stones: Influence of calcium on EPS production and biofilm formation by these isolates. Biofouling, 30(5), 547–560.

    Article  CAS  Google Scholar 

  • Luo, H., Zhu, Y. C., & Feng, X. J. (2015). Advances in bioremediation of heavy metal contaminated soils. Anhui Agricultural Science, 43(5), 224–227.

    Google Scholar 

  • Mann, S. (2001). Biomineralization: Principles and concepts in bioinorganic materials chemistry. Oxford University Press on Demand.

  • Manoli, F., Koutsopoulos, S., & Dalas, E. (1997). Crystallization of calcite on chitin. Journal of Crystal Growth, 182(1–2), 116–124.

    Article  CAS  Google Scholar 

  • Mao, X., Han, F. X., Shao, X., Guo, K., McComb, J., & Njemanze, S. (2015). Electro-kinetic enhanced phytoremediation for the restoration of multi-metal(loid) contaminated soil. International Journal of Energy, Environment and Economics, 23(3), 301–328.

    Google Scholar 

  • Mao, X., Han, F. X., Shao, X., Guo, K., McComb, J., Arslan, Z., & Zhang, Z. (2016a). Electro-kinetic remediation coupled with phytoremediation to remove lead, arsenic and cesium from contaminated paddy soil. Ecotoxicology and Environmental Safety, 125, 16–24.

    Article  CAS  Google Scholar 

  • Mao, X., Han, F. X., Shao, X., Guo, K., McComb, J., Njemanze, S., Arslan, Z., & Zhang, Z. (2016b). The distribution and elevated solubility of lead, arsenic and cesium in contaminated paddy soil enhanced with the electro-kinetic field. International Journal of Environmental Science and Technology, 13, 1641–1652.

    Article  CAS  Google Scholar 

  • Mao, X., Shao, X., Zhang, Z., & Han, F. X. (2018). Mechanism and optimization of enhanced electro-kinetic remediation on 137Cs contaminated kaolin soils: A semi-pilot study based on experimental and modeling methodology. Electrochimica Acta, 284, 38–51.

    Article  CAS  Google Scholar 

  • McKay, D. S., Gibson, E. K., Thomas-Keprta, K. L., et al. (1996). Search for past life on Mars: Possible relic biogenic activity in Martian meteorite ALH84001. Science, 273(5277), 924–930.

    Article  CAS  Google Scholar 

  • Merroun, M. L., Nedelkova, M., Ojeda, J. J., et al. (2011). Bio-precipitation of uranium by two bacterial isolates recovered from extreme environments as estimated by potentiometric titration, TEM and X-ray absorption spectroscopic analyses. Journal of Hazardous Materials, 197, 1–10.

    Article  CAS  Google Scholar 

  • Merz-Preiß, M., & Riding, R. (1999). Cyanobacterial tufa calcification in two freshwater streams: Ambient environment, chemical thresholds and biological processes. Sedimentary Geology, 126(1–4), 103–124.

    Article  Google Scholar 

  • Mitchell, A. C., & Ferris, F. G. (2006). Effect of strontium contaminants upon the size and solubility of calcite crystals precipitated by the bacterial hydrolysis of urea. Environmental Science & Ttechnology, 40(3), 1008–1014.

    Article  CAS  Google Scholar 

  • Mortensen, B. M., Haber, M. J., DeJong, J. T., et al. (2011). Effects of environmental factors on microbial induced calcium carbonate precipitation. Journal of Applied Microbiology, 111(2), 338–349.

    Article  CAS  Google Scholar 

  • Mugwar, A. J., & Harbottle, M. J. (2016). Toxicity effects on metal sequestration by microbially-induced carbonate precipitation. Journal of Hazardous Materials, 314, 237–248.

    Article  CAS  Google Scholar 

  • Mulligan, C. N., Yong, R. N., & Gibbs, B. F. (2001). Remediation technologies for metal-contaminated soils and groundwater: An evaluation. Engineering Geology, 60(1–4), 193–207.

    Article  Google Scholar 

  • Muynck, W. D., Belie, N. D., & Verstraete, W. (2010). Microbial carbonate precipitation in construction materials: A review. Ecological Engineering, 36(2), 118–136.

    Article  Google Scholar 

  • Nawarathna, T. H. K., Nakashima, K., & Kawasaki, S. (2019). Chitosan enhances calcium carbonate precipitation and solidification mediated by bacteria. International Journal of Biological Macromolecules, 133, 867–874.

    Article  CAS  Google Scholar 

  • Nilsen-Nygaard, J., Strand, S. P., Vårum, K. M., et al. (2015). Chitosan: Gels and interfacial properties. Polymers, 7(3), 552–579.

    Article  CAS  Google Scholar 

  • Omoregie, A. I., Ngu, L. H., Ong, D. E. L., et al. (2019). Low-cost cultivation of Sporosarcina pasteurii strain in food-grade yeast extract medium for microbially induced carbonate precipitation (MICP) application. Biocatalysis and Agricultural Biotechnology, 17, 247–255.

    Article  Google Scholar 

  • Oppenheimershaanan, Y., Sibonynevo, O., Bloomackermann, Z., Suissa, R., Steinberg, N., Kartvelishvily, E., Brumfeld, V., & Kolodkingal, I. (2016). Spatio-temporal assembly of functional mineral scaffolds within microbial biofilms. NPJ Biofilms & Microbiomes, 2(1), 1–10.

    Google Scholar 

  • Park, S. J., Park, Y. M., Chun, W. Y., Kim, W. J., & Ghim, S. Y. (2010). Calcite-forming bacteria for compressive strength improvement in mortar. Journal of Microbiology and Biotechnology, 20(4), 782–788.

    CAS  Google Scholar 

  • Qian, C. X., Xu, Y. B., & Hu, L. M. (2011). Study on Cu2+ in contaminated system mineralized by bacteria. Environmental Science & Technology, 34(12), 33–36.

    Google Scholar 

  • Qian, C. X., Wang, R. X., & Zhan, Q. W. (2015). Engineering application basis of microbial mineralization. Science Press.

  • Qian, X., Fang, C., Huang, M., et al. (2017). Characterization of fungal-mediated carbonate precipitation in the biomineralization of chromate and lead from an aqueous solution and soil. Journal of Cleaner Production, 164, 198–208.

    Article  CAS  Google Scholar 

  • Reddy, M. S. (2013). Biomineralization of calcium carbonates and their engineered applications: A review. Frontiers in Microbiology, 4(314), 314.

    Google Scholar 

  • Rieger, J., Frechen, T., Cox, G., Heckmann, W., Schmidt, C., & Thieme, J. (2007). Precursor structures in the crystallization/precipitation processes of CaCO3 and control of particle formation by polyelectrolytes. Faraday Discussions, 136, 265–277.

    Article  CAS  Google Scholar 

  • Rivadeneyra, M. A., Delgado, G., Ramos-Cormenzana, A., et al. (1998). Biomineralization of carbonates by Halomonas eurihalina in solid and liquid media with different salinities: Crystal formation sequence. Research in Microbiology, 149(4), 277–287.

    Article  CAS  Google Scholar 

  • Rodriguez-Navarro, C., Jroundi, F., Schiro, M., Ruiz-Agudo, E., & Gonzalez-Munoz, M. T. (2012). Influence of substrate mineralogy on bacterial mineralization of calcium carbonate: Implications for stone conservation. Applied and Environment Microbiology, 78(11), 4017–4029.

    Article  CAS  Google Scholar 

  • Roman-Ross, G., Cuello, G. J., Turrillas, X., et al. (2006). Arsenite sorption and co-precipitation with calcite. Chemical Geology, 233(3–4), 328–336.

    Article  CAS  Google Scholar 

  • Senko, J. M., Istok, J. D., Suflita, J. M., et al. (2002). In-situ evidence for uranium immobilization and remobilization. Environmental Science & Technology, 36(7), 1491–1496.

    Article  CAS  Google Scholar 

  • Shen, Y., Buick, R., & Canfield, D. E. (2001). Isotopic evidence for microbial sulphate reduction in the early Archaean era. Nature, 410(6824), 77–81.

    Article  CAS  Google Scholar 

  • Shiyab, S., Chen, J., Han, F. X., Monts, D. L., Matta, F. B., Gu, M., & Su, Y. (2009). Phytotoxicity of mercury in Indian mustard (Brassica juncea L.). Ecotoxicology and Environmental Safety, 72, 619–625.

    Article  CAS  Google Scholar 

  • Silver, S., Toth, K., & Scribner, H. (1975). Facilitated transport of calcium by cells and subcellular membranes of Bacillus subtilis and Escherichia coli. Journal of Bacteriology, 122(3), 880–885.

    Article  CAS  Google Scholar 

  • Skinner, H. C. W., & Jahren, A. H. (2007). Biomineralization. Treatise on. Geochemistry, 8(6), 1–69.

    Google Scholar 

  • Sridhar, B. B. M., Diehl, S. V., Han, F. X., Monts, D. L., & Su, Y. (2005). Anatomical changes due to uptake and accumulation of zinc and cadmium in Indian mustard (Brassica juncea). Environmental and Experimental Botany, 54, 131–141.

    Article  CAS  Google Scholar 

  • Sridhar, B. B. M., Han, F. X., Diehl, S. V., Monts, D. L., & Su, Y. (2007). Monitoring the effects of arsenic and chromium accumulation in Chinese brake fern (Pteris vittata). International Journal of Remote Sensing, 28(5), 1055–1067.

    Article  Google Scholar 

  • Stocks-Fischer, S., Galinat, J. K., & Bang, S. S. (1999). Microbiological precipitation of CaCO3. Soil Biology & Biochemistry, 31, 1563–1571.

    Article  CAS  Google Scholar 

  • Su, Y., Han, F. X., Sridhar, B. B. M., & Monts, D. L. (2005). Phytotoxicity and phytoaccumulation of trivalent and hexavalent chromium in brake fern. Environmental Toxicology and Chemistry, 24, 2019–2026.

    Article  CAS  Google Scholar 

  • Su, Y., Sridhar, B. B. M., Han, F. X., Diehl, S. V., & Monts, D. L. (2007). Effects of bioaccumulation of Cs and Sr natural isotopes on foliar structure and plant spectral reflectance of Indian mustard (Brassica juncea). Water, Air and Soil Pollution, 180, 65–74.

    Article  CAS  Google Scholar 

  • Su, Y., Han, F. X., Chen, J., Sridhar, B. B. M., & Monts, D. L. (2008). Phytoextraction and accumulation of mercury in three plant species: Indian mustard (Brassica juncea), Beard grass (Polypogon monospeliensis), and Chinese brake fern (Pteris vittata). International Journal of Phytoremediation, 10, 547–560.

    Article  CAS  Google Scholar 

  • Tourney, J., & Ngwenya, B. T. (2009). Bacterial extracellular polymeric substances (EPS) mediate CaCO3 morphology and polymorphism. Chemical Geology, 262(3–4), 138–146.

    Article  CAS  Google Scholar 

  • Tsuneda, S., Jung, J., Hayashi, H., et al. (2003). Influence of extracellular polymers on electrokinetic properties of heterotrophic bacterial cells examined by soft particle electrophoresis theory. Colloids and Surfaces B Biointerfaces, 29(2–3), 181–188.

    Article  CAS  Google Scholar 

  • Wang, K. (2018). Effects of physicochemical environmental parameters on the characteristics of calcium carbonate induced by microorganisms. Master’s thesis, Southeast University.

  • Wang, R. X., Qian, C. X., Wu, L., et al. (2007). Study on heavy metals in soil consolidated by microbial mineralization. Functional Materials, 38(9), 1523–1527.

    Article  CAS  Google Scholar 

  • Wang, M. L., Wu, S. J., & Yang, Y. Q. (2018). Microbial induced carbonate precipitation and its application for immobilization of heavy metals: A review. Research of Environmental Sciences, 31(2), 206–214.

    Google Scholar 

  • Warren, L. A., Maurice, P. A., Parmar, N., et al. (2001). Microbially mediated calcium carbonate precipitation: Implications for interpreting calcite precipitation and for solid-phase capture of inorganic contaminants. Geomicrobiology Journal, 18(1), 93–115.

    Article  CAS  Google Scholar 

  • Wei, Y. L., Chen, Z., Song, H., et al. (2019). The immobilization mechanism of U(VI) induced by Bacillus thuringiensis 016 and the effects of coexisting ions. Biochemical Engineering Journal, 144, 57–63.

    Article  CAS  Google Scholar 

  • Weiner, S., & Dove, P. M. (2003). An overview of biomineralization processes and the problem of the vital effect. Reviews in Mineralogy and Geochemistry, 54(1), 1–29.

    Article  CAS  Google Scholar 

  • Whiffin, V. S., Van Paassen, L. A., & Harkes, M. P. (2007). Microbial carbonate precipitation as a soil improvement technique. Geomicrobiology Journal, 24(5), 417–423.

    Article  CAS  Google Scholar 

  • Xu, Y. B., Qian, C. X., & Lu, Z. W. (2012). Study on the restoration of lead ion pollution by microbial mineralization. Chemical Times, 26(6), 14–17.

    CAS  Google Scholar 

  • Xu, F. Q., Dai, Q. W., Hou, L. H., et al. (2015). Isolation and Sr2+ mineralization mediated by carbonate mineralization bacteria. Geological Journal of China Universities, 21(3), 376–381.

    CAS  Google Scholar 

  • Xu, P., Fan, H., Leng, L., et al. (2020). Feasibility of microbially induced carbonate precipitation through a Chlorella-Sporosaricina co-culture system. Algal Research, 47, 101831.

    Article  Google Scholar 

  • Zamarreno, D. V., Inkpen, R., & May, E. (2009). Carbonate crystals precipitated by freshwater bacteria and their use as a limestone consolidant. Applied and Environmental Microbiology, 75(18), 5981–5990.

    Article  CAS  Google Scholar 

  • Zhang, Y., Guo, H. X., & Cheng, X. H. (2015). Role of calcium sources in the strength and microstructure of microbial mortar. Construction and Building Materials, 77, 160–167.

    Article  Google Scholar 

  • Zhang, J., Song, H., Chen, Z., et al. (2018). Biomineralization mechanism of U(VI) induced by Bacillus cereus 12–2: The role of functional groups and enzymes. Chemosphere, 206, 682–692.

    Article  CAS  Google Scholar 

  • Zhou, W. Z., Li, W. W., Zhang, Y. Z., et al. (2009). Studies on the adsorption of Pb2+ and Cu2+ by exopolysaccharides of deep-sea cold-loving bacteria Pseudoalteromonas sp. SM9913. Environmental Science, 30(1), 200–205.

    CAS  Google Scholar 

  • Zhou, X., Du, Y., & Lian, B. (2010). Effect of different culture conditions on carbonic anhydrase from Bacillus mucilaginosus inducing calcium carbonate crystal formation. Acta Microbiologica Sinica, 50(7), 955.

    CAS  Google Scholar 

  • Zhou, G. Q., Ren, Z. Y., Yang, H. Z., et al. (2013). Studies on the adsorption of heavy metal ions such as Cd2+ by microbial bacteria. Biotechnology Bulletin, 26(6), 155–159.

    Google Scholar 

  • Zhu, X. J., Li, W. L., Zhan, L., et al. (2016). The large-scale process of microbial carbonate precipitation for nickel remediation from an industrial soil. Environmental Pollution, 219, 149–155.

    Article  CAS  Google Scholar 

  • Zinjarde, S., Apte, M., Mohite, P., et al. (2014). Yarrowia lipolytica and pollutants: Interactions and applications. Biotechnology Advances, 32(5), 920–933.

    Article  CAS  Google Scholar 

  • Zou, J. L., Gu, J. F., Yang, W. T., et al. (2017). Effects of irrigation water at different pH values on bioavailability of Cd in soil and Cd content in rice. Chinese Journal of Environmental Science, 37(4), 1508–1514.

    CAS  Google Scholar 

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Funding

This study was supported by the U.S. Army Engineer Research and Development Center (W912HZ-16–2-0021), the National Natural Science Foundation of China (U1967210 and 11775106), the U.S. Nuclear Regulatory Commission (NRC-HQ-84–15-G-0042, NRC-HQ-12-G-38–0038, and NRC-HQ-84–16-G-0040), and the U.S. Department of Commerce (NOAA) (NA11SEC4810001-003499, NA16SEC4810009, NOAA Center for Coastal and Marine Ecosystems Grant # G634C22).

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Authors and Affiliations

  1. Department of Chemistry, Physics and Atmospheric Sciences, Jackson State University, Jackson, MS, 39217, USA

    Xue Chen, Dan Zhang, Jing Nie & Fengxiang X. Han

  2. School of Resource Environment and Safety Engineering, University of South China, Hengyang, 421001, China

    Xue Chen, Dan Zhang, Nan Hu & Dexin Ding

  3. U.S. Army Engineer Research and Development Center, Vicksburg, MS, 39180-6199, USA

    Steven L. Larson, John H. Ballard & Heather M. Knotek-Smith

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  1. Xue Chen
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  2. Dan Zhang
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  3. Steven L. Larson
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  4. John H. Ballard
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  5. Heather M. Knotek-Smith
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  6. Jing Nie
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  7. Nan Hu
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  8. Dexin Ding
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  9. Fengxiang X. Han
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Correspondence to Nan Hu or Fengxiang X. Han.

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Chen, X., Zhang, D., Larson, S.L. et al. Microbially Induced Carbonate Precipitation Techniques for the Remediation of Heavy Metal and Trace Element–Polluted Soils and Water. Water Air Soil Pollut 232, 268 (2021). https://doi.org/10.1007/s11270-021-05206-z

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