Hostname: page-component-586b7cd67f-t7czq Total loading time: 0 Render date: 2024-11-24T16:06:27.203Z Has data issue: false hasContentIssue false
  • English
  • Français

Bacterially Induced Mineralization of Calcium Carbonate: The Role of Exopolysaccharides and Capsular Polysaccharides

Published online by Cambridge University Press:  18 January 2007

Claudia Ercole ,
Paola Cacchio ,
Anna Lucia Botta ,
Valeria Centi  and
Aldo Lepidi
Claudia Ercole
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Paola Cacchio
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Anna Lucia Botta
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Valeria Centi
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Aldo Lepidi
Affiliation:
Department of Basic and Applied Biology, University of L'Aquila, 67010 L'Aquila, Italy
Get access

Abstract

Bacterially induced carbonate mineralization has been proposed as a new method for the restoration of limestones in historic buildings and monuments. We describe here the formation of calcite crystals by extracellular polymeric substances isolated from Bacillus firmus and Bacillus sphaericus. We isolated bacterial outer structures (glycocalix and parietal polymers), such as exopolysaccharides (EPS) and capsular polysaccharides (CPS) and checked for their influence on calcite precipitation. CPS and EPS extracted from both B. firmus and B. sphaericus were able to mediate CaCO3 precipitation in vitro. X-ray microanalysis showed that in all cases the formed crystals were calcite. Scanning electron microscopy showed that the shape of the crystals depended on the fractions utilized. These results suggest the possibility that biochemical composition of CPS or EPS influences the resulting morphology of CaCO3. There were no precipitates in the blank samples. CPS and EPS comprised of proteins and glycoproteins. Positive alcian blue staining also reveals acidic polysaccharides in CPS and EPS fractions. Proteins with molecular masses of 25–40 kDa and 70 kDa in the CPS fraction were highly expressed in the presence of calcium oxalate. This high level of synthesis could be related to the binding of calcium ions and carbonate deposition.

Keywords

bacteria glycocalyxcalcite precipitationhistoric monument protectioncalcifying bacteriaSEM
Type
Research Article
Information
Microscopy and Microanalysis , Volume 13 , Issue 1: Special Issue: Environmental, Industrial, and AppliedMicrobiology , February 2007 , pp. 42 - 50
Copyright
2007 Microscopy Society of America

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

REFERENCES

Albeck, S., Weiner, S. & Addadi, L. (1996). Polysaccharides of intracrystalline glycoproteins modulate calcite crystal growth in vitro. Chem Eur J 2, 278–284.Google Scholar
Banfield, J.F. & Hamers, R.J. (1997). Processes at minerals and surfaces with relevance to microorganisms and prebiotic synthesis. In Geomicrobiology: Interactions between Microbes and Minerals. Reviews in Mineralogy, Volume 35, Banfield, J.F. & Nealson, K.H. (Eds.), pp. 81–122. Washington, DC: Mineralogical Society of America.
Beeley, J.G. (1985). Glycoprotein and proteoglycan techniques. In Laboratory Techniques in Biochemistry and Molecular Biology, vol. 16. Burdon, R.H. & van Knippenberg, P.H. (Eds.), p. 462. Amsterdam: Elsevier.
Boquet, E., Boronat, A. & Ramos-Cormenzana, A. (1973). Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246, 527–529.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 Sed Res 72, 485–490.Google Scholar
Cacchio, P., Contento, R., Ercole, C., Cappuccio, G., Preit Martinez, M. & Lepidi, A. (2004). Involvement of microorganisms in the formation of carbonate speleothems in the cervo cave (L'Aquila-Italy). Geomicrobiol J 21, 497–509.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.Google Scholar
Castanier, S., Le Metayer-Levrel, G. & Perthuisot, J.-P. (1999). Ca-carbonates precipitation and limestone genesis—The microbiogeologist point of view. Sedim Geol 126, 9–23.Google Scholar
Chafetz, H.S. & Buczynski, C. (1992). Bacterally induced lithification of microbial mats. Palaios 7, 277–293.Google Scholar
Crayton, M.A. (1982). A comparative cytochemical study of volvocacean matrix polysaccharides. J Phycol 18, 336–344.Google Scholar
Del Gallo, M. & Haegi, A. (1990). Characterization and quantification of exocellular polysaccharides in Azospirillum brasilense and Azospirillum lipoferum. Symbiosis 9, 155–161.Google Scholar
Del Gallo, M., Negi, M. & Neyra, C.A. (1989). Calcofluor and lectin-binding exocellular polysaccharides of Azospirillum brasilense and Azospirillum lipoferum. J Bact 171, 3504–3510.Google Scholar
Dische, Z. (1962). General color reactions. Methods Carbohydr Chem 1, 477–479.Google Scholar
Douglas, S. & Beveridge, T.J. (1998). Mineral formation by bacteria in natural microbial communities. FEMS Microbiol Ecol 26, 79–88.Google Scholar
Duguid, J.P. (1951). The demonstration of bacterial capsules and slime. J Pathol Bacteriol 63, 673–685.Google Scholar
Ehrlich, H.L. (2002). Geomicrobiology, 4th ed. New York: Marcel Dekker.
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., Cappuccio, G. & Lepidi, A. (2001). Deposition of calcium carbonate in karst caves: Role of bacteria in stiffe's cave. Int J Speleol 30A, 69–79.Google Scholar
Falini, G., Albeck, S., Weiner, S. & Addadi, L. (1996). Control of aragonite or calcite polymorphism by mollusc shell macromolecules. Science 271, 67–69.Google Scholar
Ferrer, R.M., Quevedo-Sarmiento, J., Rivadeneyra, M.A., Bejar, V., Delgado, R. & Ramos-Cormenzana, A. (1988). Calcium carbonate precipitation by two groups of moderately halophilic microorganisms at different temperatures and salt concentrations. Curr Microbiol 17, 221–227.Google Scholar
Folk, R. (1993). SEM imaging of bacteria and nanobacteria in carbonate sediments and rocks. J Sedim Petrol 63, 990–999.Google Scholar
Forni, C., Haegi, A., Del Gallo, M. & Grilli Caiola, M. (1992). Production of polysaccharides by Arthrobacter globiformis associated with Anabaena azollae in Azolla leaf cavity. FEMS Microbiol Lett 93, 269–274.Google Scholar
Gonzalez-Munoz, M.T., Ben Chekroun, K., Ben Aboud, A., Arias, J.M. & Rodriguez-Gallego, M. (2000). Bacterially induced Mg-calcite formation: Role of Mg2+ in development of crystal morphology. J Sediment Res 70, 559–564.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.Google Scholar
Hirotoshi, E., Yasuaki, T., Noriaki, O., Toshihiro, K. & Toshiki, W. (2004). A crustacean Ca2+-binding protein with a glutamate-rich sequence promotes CaCO3 crystallization. Biochem J 384, 159–167.Google Scholar
Kawaguchi, T. & Decho, A.W. (2002). A laboratory investigation of cyanobacterial extracellular polymeric secretion (EPS) in influencing CaCO3 polymorphism. J Cryst Growth 240, 230–235.Google Scholar
Keefe, W.E. (1976). Formation of crystalline deposits by several genera of the family Enterobacteriaceae. Infect Immun 14, 590–592.Google Scholar
Krumbein, W.E. (1979). Photolithotrophic and chemoorganotrophic activity of bacteria and algae as related to beachrock formation and degradation (Gulf of Aqaba, Sinai). Geomicrobiol J 1, 139–203.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–685.Google Scholar
Le Mètayer-Levrel, G., Castanier, S., Orial, G., Loubière, J.F. & Perthuisot, J.P. (1999). Applications of bacterial carbonatogenesis to the protection and regeneration of limestones in buildings and historic patrimony. Sedim Geol 25–34.Google 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.Google Scholar
Macilenti, C. (2002). Indagine sui meccanismi di calcificazione promossa da batteri [Study of the mechanisms of CaCO3 precipitation by bacteria isolated in different caves] (Ph.D. Thesis). University of L'Aquila, L'Aquila-Italy.
Manca, M.C., Lama, L., Improta, R., Esposito, E., Gambacorta, A. & Nicolaus, B. (1996). Chemical composition of two exopolysaccharides from Bacillus thermoantarcticus. Appl Env Microbiol 62, 3265–3269.Google Scholar
McKay, D.S., Gibson, E.K., Thomas-Keprta, K.L., Vali, H., Romanek, C.S., Clement, S., Chiller, X.D.F, Maechling, C.R. & Zare, R.N. (1996). Search for past life on Mars: Possible relic biogenic activity in Martian meteorite ALH84001. Science 273, 924–930.Google Scholar
Monger, H.C., Daugherty, L.A., Lindemann, W.C. & Liddell, C.M. (1991). Microbial precipitation of pedogenic calcite. Geology 19, 997–1000.Google Scholar
Oliveira, M.M.M., Keim, C.N., Kurtenbach, E. & Farina, M. (2003). Mineralization of calcium carbonates in the presence of proteins from fish otoliths using an optical tweezers microscope. Acta Microscop 12(Suppl. B), 323–324.Google Scholar
Reed, W., Jane, G., Long, S., Reuber, T.L. & Walker, G.C. (1988). Analysis of the role of exopolysaccharides in Rhizobium symbiosis. In Physiology and Biochemistry of Plant Microbe Interactions, Keen, N.T., Kosuge, T. & Walling, L.L. (Eds.), pp. 51–59. Rockville, MD: American Society of Plant Physiologists.
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.Google Scholar
Rodriguez-Navarro, C., Rodriguez-Gallego, M., Ben Chekroun, K. & Gonzalez-Munoz, M.T. (2003). Conservation of ornamental stone by Myxococcus xanthus induced carbonate biomineralization. Appl Env Microbiol 69, 2182–2193.Google Scholar
Schultze-Lam, S., Harauz, G. & Beveridge, T.J. (1992). Participation of a cyanobacterial S layer in fine-grain mineral formation. J Bacteriol 174, 7971–7981.Google Scholar
Stocks-Fischer, S., Galinat, J.K. & Bang, S.S. (1999). Microbiological precipitation of CaCO3. Soil Biol Biochem 31, 1563–1571.Google Scholar
Thomas-Keprta, K.L., McKay, D.S., Wentworth, S.J., Stevens, T.O., Taunton, A.E., Allen, C., Coleman, A., Gibson, E.K. & Romanek, C.S. (1998). Bacterial mineralization patterns in basaltic aquifers: Implications for possible life in Martian meteorite ALH84001. Geology 26, 1031–1034.Google Scholar
Vali, H., McKee, M.D., Ciftcioglu, N., Sears, S.K., Plows, F.L., Chevet, E., Ghiabi, P., Plavsic, M., Kajander, O.E. & Zare, R.N. (2001). Nanoforms: A new type of protein-associated mineralization. Geoch Cosmoch Acta 65, 63–74.Google Scholar
Vasconcelos, C., McKenzie, J.A., Bernaconi, S., Grujic, D. & Tien, A.J. (1995). Microbial mediation as a possible mechanism for natural dolomite formation at low temperatures. Nature 377, 220–222.Google Scholar
Warren, L.A., Maurice, P.A., Parmar, N. & 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.Google Scholar
Whitfield, C. (1988). Bacterial extracellular polysaccharides. Can J Microbiol 34, 415–420.Google Scholar