Hostname: page-component-78c5997874-dh8gc Total loading time: 0 Render date: 2024-11-14T06:08:00.791Z Has data issue: false hasContentIssue false
  • English
  • Français

Calcium Carbonate Mineralization: Involvement of Extracellular Polymeric Materials Isolated from Calcifying Bacteria

Published online by Cambridge University Press:  15 June 2012

Claudia Ercole ,
Paola Bozzelli ,
Fabio Altieri ,
Paola Cacchio  and
Maddalena Del Gallo
Claudia Ercole*
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Paola Bozzelli
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Fabio Altieri
Affiliation:
Department of Biochemical Sciences “A. Rossi Fanelli”, Sapienza University, 00185 Rome, Italy
Paola Cacchio
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Maddalena Del Gallo
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
*
Corresponding author. E-mail: claudia.ercole@univaq.it
Get access

Abstract

This study highlights the role of specific outer bacterial structures, such as the glycocalix, in calcium carbonate crystallization in vitro. We describe the formation of calcite crystals by extracellular polymeric materials, such as exopolysaccharides (EPS) and capsular polysaccharides (CPS) isolated from Bacillus firmus and Nocardia calcarea. Organic matrices were isolated from calcifying bacteria grown on synthetic medium—in the presence or absence of calcium ions—and their effect on calcite precipitation was assessed. Scanning electron microscopy observations and energy dispersive X-ray spectrometry analysis showed that CPS and EPS fractions were involved in calcium carbonate precipitation, not only serving as nucleation sites but also through a direct role in crystal formation. The utilization of different synthetic media, with and without addition of calcium ions, influenced the biofilm production and protein profile of extracellular polymeric materials. Proteins of CPS fractions with a molecular mass between 25 and 70 kDa were overexpressed when calcium ions were present in the medium. This higher level of protein synthesis could be related to the active process of bioprecipitation.

Keywords

calcite precipitationEPSCPSbiofilmcalcifying bacteriahistoric monument protection
Type
Biological Applications: Techniques, Software, and Equipment Development
Information
Microscopy and Microanalysis , Volume 18 , Issue 4 , August 2012 , pp. 829 - 839
Copyright
Copyright © Microscopy Society of America 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Allison, D.G. & Sutherland, I.W. (1987). Role of exopolysaccharides in adhesion of freshwater bacteria. J Gen Microbiol 133, 1319–1327.Google Scholar
Anderson, S., Appanna, V.D., Huang, J. & Viswanatha, T. (1992). A novel role calcite in calcium homeostasis. FEBS Lett 308, 94–96.CrossRefGoogle ScholarPubMed
Bhaskar, P.V. & Bhosle, N.B. (2005). Microbial extracellular polymeric substances in marine biogeochemical processes. Curr Sci 88, 45–53.Google Scholar
Bouquet, E., Boronat, A. & Ramos-Cormenzana, A. (1973). Production of calcite (calcium carbonate) crystal by soil bacteria is a general phenomenon. Nature 246, 527–529.CrossRefGoogle Scholar
Boyd, A. & Chakrabarty, A.M. (1995). Pseudomonas aeruginosa biofilms: Role of the alginate exopolysaccharide. J Ind Microbiol 15, 162–168.CrossRefGoogle ScholarPubMed
Bozzelli, P. (2011). Utilizzo di batteri calcificanti per il biorecupero dei beni culturali [Utilization of calcifying bacteria for the bioremediation of cultural heritage]. PhD Thesis. University of L'Aquila, L'Aquila-Italy. Google Scholar
Braissant, O., Cailleau, G., Dupraz, C. & Verrecchia, E.P. (2003). Bacterially induced mineralization of calcium carbonate in terrestrial environments: The role of exopolysaccharides and amino acid. J Sediment Res 73(3), 485–490.Google Scholar
Cacchio, P., Ercole, C., Cappuccio, G. & Lepidi, A. (2003). Calcium carbonate precipitation by bacterial strains isolated from a limestone cave and from a loamy soil. Geomicrobiol J 20, 85–98.CrossRefGoogle Scholar
Castanier, S., Le Metayer-Levrel, G. & Perthuisot, J.P. (1999). Ca-carbonates precipitation and limestone genesis—The microbiogeologist point of view. Sediment Geol 126, 9–23.CrossRefGoogle Scholar
Castanier, S., Le Metayer-Levrel, G. & Perthuisot, J.P. (2000). Bacterial roles in the precipitation of carbonate minerals. In Microbial Sediments, Riding, R. & Awramik, S.M. (Eds.), pp. 32–39. Berlin: Springer-Verlag.Google Scholar
Conway, B.D., Venu, V. & Speert, D.P. (2002). Biofilm formation and acyl homoserine lactone production in the Burkholderia cepacia complex. J Bacteriol 184 (20), 5678–5685.Google Scholar
Decho, A.W. (2009). Overview of biopolymer-induced mineralization: What goes on in biofilms? Ecol Eng 30, 1–8.Google Scholar
Dick, J., De Windt, W., De Graef, B., Saveyn, H., Ven 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.CrossRefGoogle ScholarPubMed
Dische, Z. (1962). General color reactions. Method Carbohyd Chem 1, 477–479.Google Scholar
Dittrich, M. & Sibler, S. (2010). Calcium carbonate precipitation by cyanobacterial polysaccharides. In Tufas and Speleothems: Unravelling the Microbial and Physical Controls, Pedley, H.M. & Rogerson, M. (Eds.), Special Publications 336, pp. 51–63. London: Geological Society.Google Scholar
Douglas, S. & Beveridge, T.J. (1998). Mineral formation by bacteria in natural microbial communities. FEMS Microbiol Ecol 26, 79–88.Google Scholar
Dupraz, C., Reid, R.P., Braissant, O., Decho, A.W., Norman, R.S. & Visscher, P.T. (2009). Processes of carbonate precipitation in modern microbial mats. Earth Sci Rev 96, 141–162.Google Scholar
Ercole, C., Altieri, F., Piccone, C., Del Gallo, M. & Lepidi, A. (1999). Influence of mangnese dioxide and manganic ions on the production of two proteins in Arthrobacter sp. Geomicrobiol J 16, 95–103.Google Scholar
Ercole, C., Cacchio, P., Botta, A.L., Centi, V. & Lepidi, A. (2007). Bacterially induced mineralization of calcium carbonate: The role of exopolysaccharides and capsular polysaccharides. Microsc Microanal 13, 42–50.CrossRefGoogle ScholarPubMed
Erlich, H.L. (1996). Geomicrobiology, 3rd ed. New York: Marcel Dekker.Google Scholar
Ferrer, M.R., Quevedo-Sarmiento, J., Rivadeneyra, M.A., Bejar, V., Delgado, G. & Ramos-Coemenzana, A. (1988). Calcium carbonate precipitation by two group of moderately halophilic microorganisms at different temperatures and salt concentrations. Curr Microbiol 17, 221–227.CrossRefGoogle Scholar
González-Muñoz, M.T., Rodriguez-Navarro, C., Martínez-Ruiz, F., Arias, J.M., Merroun, M.L. & Rodriguez-Gallego, M. (2010). Bacterial biomineralization: New insights from Myxococcus-induced mineral precipitation. In Tufas and Speleothems: Unravelling the Microbial and Physical Controls, Pedley, H.M. & Rogerson, M. (Eds.), Special Publications 336, pp. 31–50. London: Geological Society.Google Scholar
Hammes, F., Boon, N., De Villiers, J., Verstraete, W. & Siciliano, S.D. (2003). Strain-specific ureolytic microbial calcium carbonate precipitation. Appl Environ Microb 69, 4901–4909.CrossRefGoogle ScholarPubMed
Hammes, F. & Verstraete, W. (2002). Key roles of pH and calcium metabolism in microbial carbonate precipitation. In Reviews in Environmental Science & Biotechnology, 1, 3–7. The Netherlands: Kluwer Academic Publishers.Google Scholar
Kawaguchi, T. & Decho, A.W. (2002). A laboratory investigation of cyanobacterial extracellular polymeric secretions (EPS) in influencing CaCO3 polymorphism. J Cryst Growth 240, 230–235.CrossRefGoogle Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.CrossRefGoogle ScholarPubMed
Le Mètayer-Levrel, G., Castanier, S., Orial, G., Loubiere, J.F. & Perthuisot, J.P. (1999). Applications of bacterial carbonatogenesis to the protection and regeneration of limestones in buildings and historic patrimony. Sediment Geol 126, 25–34.CrossRefGoogle Scholar
Lian, B., Hu, Q., Chen, J., Ji, J. & Teng, H.H. (2006). Carbonate biomineralization induced by soil bacterium Bacillus megaterium . Geochim Cosmochim Ac 70, 5522–5535.CrossRefGoogle Scholar
Lowry, O.H., Rosebrough, M.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with Folin phenol reagent. J Biol Chem 193, 265–275.CrossRefGoogle ScholarPubMed
Macilenti, C. (2002). Indagine sui meccanismi di calcificazione promossa da batteri [Study of the mechanisms of CaCO3 precipitation by bacteria isolated in different caves]. PhD Thesis. University of L'Aquila, L'Aquila-Italy. Google Scholar
McConnaughey, T.A. & Whelan, F.F. (1997). Calcification generates protons for nutrient and bicarbonate uptake. Earth Sci Rev 42, 95–117.CrossRefGoogle Scholar
Merz-Preiss, M. & Riding, R. (1999). Cyanobacterial tufa calcification in two freshwater streams: Ambient environment, chemical thresholds and biological processes. Sediment Geol 126 (1-4), 103–124.CrossRefGoogle Scholar
Michiels, J., Xi, C., Verhaert, J. & Vanderleyden, J. (2002). The functions of Ca2+ in bacteria: A role for EF-hand proteins? Trends Microbiol 10(2), 87–93.CrossRefGoogle ScholarPubMed
Morita, R.Y. (1980). Calcite precipitation by marine bacteria. Geomicrobio J 2, 63–82.CrossRefGoogle Scholar
Nichols, P.D. & Nichols, C.A.M. (2008). Microbial signature lipid profiling and exopolysaccharides: Experiences initiated with Professor David C. White and transported to Tasmania, Australia. J Microbiol Meth 74, 33–46.CrossRefGoogle Scholar
Nielsen, P.H. & Jahn, A. (1999). Extraction of EPS. In Microbial Extracellular Polymeric Substances: Characterization, Structure, and Function, Wingender, J., Neu, T.R. & Flemming, H.C. (Eds.), pp. 49–72. Berlin, Heidelberg: Springer.CrossRefGoogle Scholar
Norris, V., Grant, S., Freestone, P., Canvin, J., Sheikh, F.N., Toth, I., Trinei, M., Modha, K. & Norman, R.I. (1996). Calcium signalling in bacteria. J Bacteriol 178(13), 3677–3682.CrossRefGoogle ScholarPubMed
Novitsky, J.A. (1981). Calcium carbonate precipitation by marine bacteria. Geomicrobiol J 2, 63–82.CrossRefGoogle Scholar
Onek, L.A. & Smith, R.J. (1992). Calcium and calcium mediated regulation in prokaryotes. J Gen Microbiol 138, 1039–1049.CrossRefGoogle ScholarPubMed
O'Toole, G.A. & Kolter, R. (1998). Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: A genetic analysis. Mol Microbiol 28, 449–461.Google Scholar
Papida, S., Murphy, W. & May, E. (2000). Enhancement of physical weathering of building stones by microbial populations. Int Biodeter Biodegr 46, 305–317.CrossRefGoogle Scholar
Patrauchan, M.A., Sarkisova, S., Sauer, K. & Franklin, M.J. (2005). Calcium influences cellular and extracellular product formation during biofilm-associated growth of a marine Pseudoalteromonas sp. Microbiology 151, 2885–2897.CrossRefGoogle ScholarPubMed
Perry, T.D., McNamara, C., Mitchell, R. & Hernandez-Duque, G. (2003). An investigation of bacterial dissolution of Maya limestone: Biodiversity and functional analysis. In Molecular Biology and Cultural Heritage: Proceedings of the International Conference, Sevilla, Spain, March 4–7, 2003, Saiz-Jimenez, C. (Ed.), pp. 137–140. Rotterdam, The Netherlands: A. A. Balkema Publishers.Google Scholar
Rivadeneyra, M.A., Delgado, R., Del Moral, A., Ferrer, M.R. & Ramos-Cormenzana, A. (1994). Precipitation of calcium carbonate by Vibrio spp. from an inland saltern. FEMS Microbiol Ecol 13, 197–204.CrossRefGoogle Scholar
Rivadeneyra, M.A., Delgado, G., Ramos-Cormenzana, A. & Delgado, R. (1998). Biomineralization of carbonates by Halomonas eurihalina in solid and liquid media with different salinities: Crystal formation sequence. Res Microbiol 149, 277–287.CrossRefGoogle ScholarPubMed
Rivadeneyra, M.A., Párraga, J., Delgado, R., Ramos-Cormenzana, A. & Delgado, G. (2004). Biomineralization of carbonates by Halobacillus trueperi in solid and liquid media with different salinities. FEMS Microbiol Ecol 48, 39–46.CrossRefGoogle ScholarPubMed
Rivadeneyra, M.A., Ramos-Cormenzana, A., Delgado, G. & Delgado, R. (1996). Process of carbonate precipitation by Deleya halophila . Curr Microbiol 32, 308–313.Google Scholar
Sarró, M.I., Garcia, A.M., Rivalta, V.M., Moreno, D. & Arroyo, I. (2006). Biodeterioration of the Lions Fountain at the Alhambra Palace, Granata, Spain. Build Environ 41, 1811–1820.CrossRefGoogle Scholar
Schultze-Lam, S., Fortin, D., Davis, B.S., Beveridge, T.J. (1996). Mineralisation of bacterial surfaces. Chem Geol 132, 171–181.Google Scholar
Shemarova, I.V. & Nesterov, V.P. (2005). Evolution of mechanisms of Ca2+-signaling: Role of calcium ions in signal transduction in prokaryotes. J Evol Biochem Phys 41(1), 12–19.CrossRefGoogle Scholar
Straley, S.C., Plano, G.V., Skrzypek, E., Haddix, P.L. & Fields, K.A. (1993). Regulation by Ca2+ in the Yersinia low-Ca2+ response. Mol Microbiol 8, 1005–1010.CrossRefGoogle ScholarPubMed
Sutherland, I.W. (2001). Biofilm exopolysaccharides: A strong and sticky framework. Microbiology 147, 3–9.CrossRefGoogle Scholar
Thimodo, M. (2007). A lux/gfp dual label system for studying attachment and biofilm formation of Enterobacter sakazakii . Surg 1, 22–28.Google Scholar
Tisa, L.S. & Adler, J. (1995). Cytoplasmic free-Ca2+ level rises with repellents and falls with attractans in Escherichia coli chemotaxis. Proc Natl Acad Sci USA 92, 10777–10781.Google Scholar
Trombe, M.C., Rieux, V. & Baille, F. (1994). Mutation which alter the kinetics of calcium transport alter the regulation of competence in Streptococcus pneumoniae . J Bacteriol 176 (7), 1992–1996.Google Scholar
Warscheid, T. & Braams, J. (2000). Biodeterioration of stone: A review. Int Biodeter Biodegr 46, 343–368.Google Scholar
Watnick, P.I. & Kolter, R. (1999). Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol 34, 586–595.Google Scholar
Yu, X.C. & Margolin, W. (1997). Ca2+-mediated GTP-dependent dynamic assembly of bacterial cell division protein FtsZ into asters and polymer networks in vitro. Embo J 16, 5455–5463.CrossRefGoogle ScholarPubMed
Zamarreño, D.V., Inkpen, R. & May, E. (2009). Carbonate crystals precipitated by freshwater bacteria and their use as a limestone consolidant. Appl Environ Microb 75, 5981–5990.Google Scholar
Zanardini, E., Abbruscato, P., Scaramelli, L., Onelli, E., Realini, M., Patrignani, G. & Sorlini, C. (2002). Red stains on Carrara marble: A case study of the Certosa of Pavia, Italy. In Art Biology and Conservation: Biodeterioration of Works of Art, Koestler, R.J., Koestler, V.H., Charola, A.E. & Nieto-Fernandez, F.E. (Eds.), pp. 226–247. New York: The Metropolitan Museum of Art Publishing.Google Scholar