Skip to main content
SpringerLink
Log in

New insights into the role of pH and aeration in the bacterial production of calcium carbonate (CaCO3)

  • Biotechnological products and process engineering
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Over recent years, the implementation of microbially produced calcium carbonate (CaCO3) in different industrial and environmental applications has become an alternative for conventional approaches to induce CaCO3 precipitation. However, there are many factors affecting the biomineralization of CaCO3, which may restrict its application. In this study, we investigated the effects of pH and aeration as the main two influential parameters on bacterial precipitation of CaCO3. The results showed that the aeration had a significant effect on bacterial growth and its rise from 0.5 to 4.5 SLPM could produce 4.2 times higher CaCO3 precipitation. The increase of pH to 12 resulted in 6.3-fold increase in CaCO3 precipitation as compared to uncontrolled-pH fermentation. Morphological characterization showed that the pH is an effective parameter on CaCO3 morphology. Calcite was found to be the predominant precipitate during aeration-controlled fermentations, while vaterite was mainly produced at lower pH (up to 10) over controlled-pH fermentations. Further increase in pH resulted in a morphological transition, and vaterite transformed to calcite at the pH ranges between 10 and 12.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Banks ED, Taylor NM, Gulley J, Lubbers BR, Giarrizo JG, Bullen HA, Hoehler TM, Barton HA (2010) Bacterial calcium carbonate precipitation in cave environments: a function of calcium homeostasis. Geomicrobiol J 27:444–454

    Article  CAS  Google Scholar 

  • Barton LL, Northup DE (2011) Microbes at work in nature: biomineralization and microbial weathering. In: microbial ecology. John Wiley & Sons, Inc, Hoboken

    Google Scholar 

  • Berenjian A, Mahanama R, Talbot A, Regtop H, Kavanagh J, Dehghani F (2012) Advances in menaquinone-7 production by bacillus subtilis natto: fed-batch glycerol addition. Am J Biochem Biotechnol 8:105–110

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Burbank MB, Weaver TJ, Green TL, Williams B, Crawford RL (2011) Precipitation of calcite by indigenous microorganisms to strengthen liquefiable soils. Geomicrobiology J 28:301–312

    Article  Google Scholar 

  • Burne RA, Chen YYM (2000) Bacterial ureases in infectious diseases. Microbes Infect 2:533–542

    Article  CAS  PubMed  Google Scholar 

  • Çalík P, Çalík G, Özdamar TH (1998) Oxygen transfer effects in serine alkaline protease fermentation by Bacillus licheniformis: use of citric acid as the carbon source. Enzyme Microb Tech 23:451–461

    Article  Google Scholar 

  • Castainer S, Metayer-Levrel GL, Perthuisot JP (1999) Ca-carbonates precipitation and limestone genesis-the microbiogeologist point of view. Sediment Geol 126:9–23

    Article  Google Scholar 

  • Castainer S, Metayer-Levrel GL, Perthuisot J (2000) Bacterial roles in the precipitation of carbonate minerals. In: Riding RE, Awramik SM (eds) Microbial sediments. Springer, Berlin Heidelberg, pp 32–39

    Chapter  Google Scholar 

  • Da Silva FB, De Belie N, Boon N, Verstraete W (2015) Production of non-axenic ureolytic spores for self-healing concrete applications. Constr Build Mater 93:1034–1041

    Article  Google Scholar 

  • DeJong JT, Fritzges MB, Nüsslein K (2006) Microbially induced cementation to control sand response to undrained shear. J Geotech Geoenviron 132:1381–1392

    Article  CAS  Google Scholar 

  • De Muynck W, Cox K, Belie ND, Verstraete W (2008) Bacterial carbonate precipitation as an alternative surface treatment for concrete. Constr Build Mater 22:875–885

    Article  Google Scholar 

  • Dick J, De Windt W, De Graef B, Saveyn H, Van Der Meeren P, De Belie N, Verstraete W (2006) Bio-deposition of a calcium carbonate layer on degraded limestone by Bacillus species. Biodegradation 17:357–367

    Article  CAS  PubMed  Google Scholar 

  • Folk RL (1994) Interaction between bacteria, nannobacteria, and mineral precipitation in hot springs of central Italy. Geogr phys Quatern 48:233–246

    Google Scholar 

  • Fujita Y, Ferris FG, Lawson RD, Colwell FS, Smith RW (2000) Calcium carbonate precipitation by ureolytic subsurface bacteria. Geomicrobiol J 17:305–318

    Article  CAS  Google Scholar 

  • Gat D, Tsesarsky M, Shamir D, Ronen Z (2014) Accelerated microbial-induced CaCO3 precipitation in a defined coculture of ureolytic and non-ureolytic bacteria. Biogeosciences 11:2561–2569

    Article  CAS  Google Scholar 

  • Hammes F, 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 

  • Hu YB, Wolthers M, Wolf-Gladrow DA, Nehrke G (2015) Effect of pH and phosphate on calcium carbonate polymorphs precipitated at near-freezing temperature. Cryst Growth Des 15:1596–1601

    Article  CAS  Google Scholar 

  • Jiménez-López C, Caballero E, Huertas FJ, Romanek CS (2001) Chemical, mineralogical and isotope behavior, and phase transformation during the precipitation of calcium carbonate minerals from intermediate ionic solution at 25 °C. Geochim Cosmochim Ac 65:3219–3231

    Article  Google Scholar 

  • Jimenez-Lopez C, Rodriguez-Navarro A, Dominguez-Vera JM, Garcia-Ruiz JM (2003) Influence of lysozyme on the precipitation of calcium carbonate: a kinetic and morphologic study. Geochim Cosmochim Ac 67:1667–1676

    Article  CAS  Google Scholar 

  • Kaur N, Reddy MS, Mukherjee A (2013) Biomineralization of calcium carbonate polymorphs by the bacterial strains isolated from calcareous sites. J Microbiol Biotechn 23:707–714

    Article  Google Scholar 

  • Kim HJ, Eom HJ, Park C, Jung J, Shin B, Kim W, Chung N, Choi I, Park W (2015) Calcium carbonate precipitation by Bacillus and sporosarcina strains isolated from concrete and analysis of the bacterial community of concrete. J Microbiol Biotechn 26:540–548

    Article  Google Scholar 

  • Kremer B, Kazmierczak J, Stal LJ (2008) Calcium carbonate precipitation in cyanobacterial mats from sandy tidal flats of the North Sea. Geobiology 6:46–56

    CAS  PubMed  Google Scholar 

  • Loewenthal RE, Marais GVR (1978) Carbonate chemistry of aquatic systems: theory and application. Ann Arbor Science publishers Inc., Ann Arbor

    Google Scholar 

  • Ma YF, Gao YH, Feng QL (2010) Effects of pH and temperature on CaCO3 crystallization in aqueous solution with water soluble matrix of pearls. J Cryst Growth 312:165–3170

    Article  Google Scholar 

  • Mitchell AC, Dideriksen K, Spangler LH, Cunningham AB, Gerlach R (2010) Microbially enhanced carbon capture and storage by mineral-trapping and solubility-trapping. Envir Sci Tech Lib 44:5270–5276

    Article  CAS  Google Scholar 

  • Onal Okyay T, Frigi Rodrigues D (2014) Optimized carbonate micro-particle production by Sporosarcina pasteurii using response surface methodology. Ecol Eng 62:168–174

    Article  Google Scholar 

  • Ramachandran SK, Ramakrishnan V, Bang SS (2001) Remediation of concrete using micro-organisms. ACI Mater J 98:3–9

    CAS  Google Scholar 

  • Rivadeneyra MA, Delgado R, del Moral A, Ferrer MR, Ramos-Cormenzana A (1994) Precipatation of calcium carbonate by Vibrio spp. from an inland saltern. FEMS Microbiol Ecol 13:197–204

    Article  CAS  Google Scholar 

  • Ronholm J, Schumann D, Sapers HM, Izawa M, Applin D, Berg B, Mann P, Vali H, Flemming RL, Cloutis EA, Whyte LG (2014) A mineralogical characterization of biogenic calcium carbonates precipitated by heterotrophic bacteria isolated from cryophilic polar regions. Geobiology 12:542–556

    Article  CAS  PubMed  Google Scholar 

  • Rusznyák A, Akob DM, Nietzsche S, Eusterhues K, Totsche KU, Neu TR, Frosch T, Popp J, Keiner R, Geletneky J, Katzschmann L, Schulze E, Küsel K (2012) Calcite biomineralization by bacterial isolates from the recently discovered pristine karstic Herrenberg cave. Appl Environ Microb 78:1157–1167

    Article  Google Scholar 

  • Sarda D, Choonia HS, Sarode DD, Lele SS (2009) Biocalcification by Bacillus pasteurii urease: a novel application. J Ind Microbiol Biot 36:1111–1115

    Article  CAS  Google Scholar 

  • Seifan M, Samani AK, Berenjian A (2016a) Bioconcrete: next generation of self-healing concrete. Appl Microbiol Biotechnol 100:2591–2602

    Article  CAS  PubMed  Google Scholar 

  • Seifan M, Samani AK, Berenjian A (2016b) Induced calcium carbonate precipitation using Bacillus species. Appl Microbiol Biotechnol 100:9895–9906

    Article  CAS  PubMed  Google Scholar 

  • Stocks-Fischer S, Galinat JK, Bang SS (1999) Microbiological precipitation of CaCO3. Soil Biol Biochem 31:1563–1571

    Article  CAS  Google Scholar 

  • Tiano P, Biagiotti L, Mastromei G (1999) Bacterial bio-mediated calcite precipitation for monumental stones conservation: methods of evaluation. J Microbiol Meth 36:139–145

    Article  CAS  Google Scholar 

  • Tourney J, Ngwenya BT (2009) Bacterial extracellular polymeric substances (EPS) mediate CaCO3 morphology and polymorphism. Chem Geol 262:138–146

    Article  CAS  Google Scholar 

  • Van Hamme JD, Singh A, Ward OP (2003) Recent advances in petroleum microbiology. Microbiol Mol biol R 67:503–549

    Article  CAS  Google Scholar 

  • Van Paassen LA, Daza CM, Staal M, Sorokin DY, van der Zon W, van Loosdrecht Mark CM (2010) Potential soil reinforcement by biological denitrification. Ecol Eng 36:168–175

    Article  Google Scholar 

  • Wang X, Sun H, Xia Y, Chen C, Xu H, Shan H, Lu JR (2009) Lysozyme mediated calcium carbonate mineralization. J Colloid Interf Sci 332:96–103

    Article  CAS  Google Scholar 

  • Wang JY, Soens H, Verstraete W, De Belie N (2014b) Self-healing concrete by use of microencapsulated bacterial spores. Cement Concrete res 56:139–152

    Article  CAS  Google Scholar 

  • Wang J, Dewanckele J, Cnudde V, Van Vlierberghe S, Verstraete W, De Belie N (2014a) X-ray computed tomography proof of bacterial-based self-healing in concrete. Cement Concrete Comp 53:289–304

    Article  CAS  Google Scholar 

  • Warren LA, Maurice PA, Parmar N, Ferris GF (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 

  • Wei S, Cui H, Jiang Z, Liu H, He H, Fang N (2015) Biomineralization processes of calcite induced by bacteria isolated from marine sediments. Braz J Microbiol 46:455–464

    Article  PubMed  PubMed Central  Google Scholar 

  • Wiktor V, Jonkers HM (2011) Quantification of crack-healing in novel bacteria-based self-healing concrete. Cement Concrete Comp 33:763–770

    Article  CAS  Google Scholar 

  • Wilks JC, Kitko RD, Cleeton SH, Lee GE, Ugwu CS, Jones BD, Bondurant SS, Slonczewski JL (2009) Acid and base stress and transcriptomic responses in Bacillus subtilis. Appl Environ Microb 75:981–990

    Article  CAS  Google Scholar 

  • Zhang JL, Wang CG, Wang QL, Feng JL, Pan W, Zheng XC, Liu B, Han NX, Xing F, Deng X (2016) A binary concrete crack self-healing system containing oxygen-releasing tablet and bacteria and its Ca2+-precipitation performance. Appl Microbiol Biotechnol 100:10295–10306

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This investigation was financially supported by The University of Waikato, New Zealand.

Author information

Authors and Affiliations

  1. School of Engineering, Faculty of Science and Engineering, The University of Waikato, Hamilton, New Zealand

    Mostafa Seifan, Ali Khajeh Samani & Aydin Berenjian

Authors
  1. Mostafa Seifan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ali Khajeh Samani
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aydin Berenjian
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aydin Berenjian.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study does not contain any studies with human participants or animals performed by any of the authors.

Electronic supplementary material

ESM 1

(PDF 80 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seifan, M., Samani, A.K. & Berenjian, A. New insights into the role of pH and aeration in the bacterial production of calcium carbonate (CaCO3). Appl Microbiol Biotechnol 101, 3131–3142 (2017). https://doi.org/10.1007/s00253-017-8109-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-017-8109-8

Keywords

Search

Navigation