Hostname: page-component-78c5997874-94fs2 Total loading time: 0 Render date: 2024-11-17T18:23:09.821Z Has data issue: false hasContentIssue false

Synchrotron X-Ray Microanalysis and Imaging of Synthetic Biological Calcium Carbonate in Comparison With Archaeological Samples Originating from the Large Cave of Arcy-sur-Cure (28000-24500 BP, Yonne, France)

Published online by Cambridge University Press:  04 September 2013

Emilie Chalmin*
Affiliation:
European Synchrotron Radiation Facility, Polygone Scientifique Louis Neel -6, rue Jules Horowitz - 38000 Grenoble, France EDYTEM, UMR 5204 CNRS, Université de Savoie, Technolac, 73376 Le Bourget du Lac, France
Ina Reiche
Affiliation:
Laboratoire d'Archéologie Moléculaire et Structurale (LAMS), UMR 8220 CNRS, University Pierre and Marie Curie (UPMC) Paris VI, 75005 Paris, France
*
*Corresponding author. E-mail: [email protected]
Get access

Abstract

Biosynthetic calcite samples were investigated using combined synchrotron X-ray microspectroscopy mapping. These samples were prepared with bacteria isolated from the Large cave of Arcy-sur-Cure in which prehistoric figures are masked by an opaque calcite layer. The biotic or abiotic origin of this layer is the issue of the present work. As previously known, a large community of bacteria may be involved in the CaCO3 formation in caves. A mixture of calcite/vaterite was obtained from bacteria isolated from the cave. Therefore, we can offer conclusions on their calcifying capability. The rare presence of vaterite in cave environments may be treated as a marker of biotic carbonate formations. Moreover, an amorphous calcium phosphate phase was present in the form of a calcite/vaterite mixture in the biotic model samples. This mixture of phases could be used as a tracer of the biotic process of CaCO3 formation. These biotic tracer phases were not identified using the applied analytical methods in the natural samples taken from the opaque calcite layers that covered the prehistoric figures of the Large cave. In this case, based on the obtained results, the biotic calcite formation process is likely to be considered as an undetectable effect at minimum.

Type
Biomedical and Biological Applications
Copyright
Copyright © Microscopy Society of America 2013 

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

Adolphe, J.P. & Billy, C. (1974). Biosynthèse de calcite par une association bactérienne aérobie. CR de l'Académie des Sciences, Paris 278, 28732875.Google Scholar
Adolphe, J.P., Paradas, J. & Soleilhavoup, F. (1994). An example of carbonate biosynthesis in karst. In Breakthroughs in Karst Geomicrobiology and Redox Geochemistry, Sasowsky, I.D. & Palmer, M.V. (Eds.), p. 2. Colorado Spring, CO: Karst Waters Institute.Google Scholar
Alcocer, J., Lugo, A., Del Rosario Sanchez, M., Escobar, E. & Sanchez, M. (1999). Bacterioplankton from cenotes and anchialine caves of Quintant Roo, Yucatan Peninsula, Mexico. Rev Biol Trop 47, 1925.Google Scholar
Appanna, V.D., Anderson, S.L. & Skakoon, T. (1997). Biogenesis of calcite: A biochemical model. Microbiol Res 152, 341343.CrossRefGoogle Scholar
Bachmeier, K.L., Williams, A.E., Warmington, J.R. & Bang, S.S. (2002). Urease activity in microbiologically-induced calcite precipitation. J Biotechnol 93, 171181.CrossRefGoogle ScholarPubMed
Baffier, D., Girard, M., Menu, M. & Vignaud, C. (1999). La couleur à la Grande Grotte d'Arcy-sur-Cure (Yonne). L'anthropologie Tome 103, 121.Google Scholar
Bastian, F., Alabouvette, C., Jurado, V. & Saiz-Jimenez, C. (2009a). Impact of biocide treatments on the bacterial communities of the Lascaux cave. Naturwissenschaften 96, 863868.CrossRefGoogle ScholarPubMed
Bastian, F., Alabouvette, C. & Saiz-Jimenez, C. (2009b). The impact of arthropods on fungal community structure in Lascaux cave. J Appl Microbiol 106, 14561462.Google Scholar
Bastian, F., Jurado, V., Novakova, A., Alabouvette, C. & Saiz-Jimenez, C. (2010). The microbiology of Lascaux cave. Microbiology 156, 644652.Google Scholar
Ben Chekroun, K., Rodriguez-Navarro, C., Gonzalez-Munoz, M.T., Arias, J.M., Cultrone, G. & Rodriguez-Gallego, M. (2004). Precipitation and growth morphology of calcium carbonate induced by Myxococcus xanthus: Implications for recognition of bacterial carbonates. J Sediment Res 74, 868876.CrossRefGoogle Scholar
Benzerara, K., Menguy, N., Guyot, F., Skouri, F., de Luca, G., Barakat, M. & Heulin, T. (2004). Biologically controlled precipitation of calcium phosphate by Ramlibacter tataouinensis . Earth Planet Sci Lett 228, 439449.CrossRefGoogle Scholar
Boquet, E., Boronat, A. & Ramos-Cormenzana, A. (1973). Production of calcite (calcium carbonate) crystals by soil bacteria is a general phenomenon. Nature 246, 527529.CrossRefGoogle Scholar
Bourdin, C.M., Douville, E. & Genty, D. (2011). Alkaline-earth metal and rare-earth element incorporation control by ionic radius and growth rate on a stalagmite from the Chauvet cave, Southeastern France. Chem Geol 290, 111.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 acids. J Sediment Res 73, 485490.Google Scholar
Cacchio, P., Contento, R., Ercole, C., Cappuchio, G., Martinez, M. & Lepidi, A. (2004). Involvement of microorganisms in the formation of carbonate speleothems in the Cervo cave (l'Aquila, Italy). Geomicrobiol J 21, 497509.CrossRefGoogle 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, 8598.Google Scholar
Canaveras, J.C., Hoyos, M., Sanchez-Moral, S., Sanz-Rubio, E., Bedoya, J., Soler, V., Groth, I., Schumann, P., Laiz, L., Gonzalez, I. & Saiz-Jimenez, C. (1999). Microbial communities associated with hydromagnesite and needle-fiber aragonite deposits in a Karstic cave (Altamira, Northern Spain). Geomicrobiol J 16, 925.Google Scholar
Castanier, S., Le Métayer-Levrel, G. & Perthuisot, J.-P. (1999). Ca-carbonates precipitation in limestone genesis—the microgeobiologist point of view. Sediment Geol 126, 923.CrossRefGoogle Scholar
Chafetz, H.S., Rush, P.F. & Utech, N.M. (1991). Microenvironmental controls on mineralogy and habit of CaCO3 precipitates: An example from an active travertine system. Sedimentology 38, 107126.Google Scholar
Chalmin, E., D'Orlyé, F., Zinger, L., Charlet, L., Geremia, R., Orial, G., Menu, M., Baffier, D. & Reiche, I. (2007). Biotic vs. abiotic calcite formation on prehistoric cave paintings: The case of Arcy-sur-Cure “Grande Grotte” (Yonne, France,). Geol Soc Lond 279, 185197.Google Scholar
Chalmin, E., Perrette, Y., Fanget, B. & Susini, J. (2013). Investigation of organic matter trapped in synthetic carbonates. Microsc Microanal 19, 132144.Google Scholar
Chalmin, E., Sansot, E., Orial, G., Bousta, F. & Reiche, I. (2008). Microanalysis and synthesis of calcite. Growth mechanisms on prehistoric paintings in the “Large cave”, Arcy-sur-Cure (Yonne, France). X-Ray Spectrom 37, 424434.CrossRefGoogle Scholar
Cotte, M., Welcomme, E., Solé, V.A., Salomé, M., Menu, M., Walter, P. & Susini, J. (2007). Synchrotron-based X-ray spectromicroscopy used for the study of an atypical micrometric pigment in 16th century paintings. Anal Chem 79, 69886994.CrossRefGoogle Scholar
Couradeau, E., Benzerara, K., Gérard, E., Moreira, D., Bernard, S., Brown, G.E. & Lopez-Garcia, P. (2012). An early-branching microbialite cyanobacterium forms intracellular carbonates. Science 336, 459462.Google Scholar
Cuezva, S., Sanchez-Moral, S., Saiz-Jimenez, C. & Canaveras, J.C. (2009). Microbial communities and associated mineral fabrics in Altamira cave, Spain. Int J Speleol 38, 8392.Google Scholar
De Andrade, V., Susini, J., Salomé, M., Beraldin, O., Rigault, C., Heymes, T., Lewin, E. & Vidal, O. (2011). Submicrometer hyperspectral X-ray imaging of heterogeneous rocks and geomaterials: Applications at the Fe K-edge. Anal Chem 83, 42204227.CrossRefGoogle ScholarPubMed
Delgado, G., Parraga, J., Martin-Garcia, J.M., de las Angustias Rivadeneyra, M., Sanchez-Maranon, M. & Delgado, R. (2012). Carbonate and phosphate precipitation by saline soil bacteria in a monitored culture medium. Geomicrobiol J 30, 199208.Google Scholar
Dittrich, M., Müller, B., Mavrocordatos, D. & Wehrli, B. (2003). Induced calcite precipitation by cyanobacterium Synechococcus. Acta Hydrochim Hydrobiol 31, 162169.CrossRefGoogle Scholar
Dittrich, M. & Obst, M. (2004). Are picoplankton responsible for calcite precipitation in lakes? Ambio 33, 559564.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, 5163. Geological Society of London.Google Scholar
Dupraz, S., Parmentier, M., Ménez, B. & Guyot, F. (2009). Experimental and numerical modeling of bacterially induced pH increase and calcite precipitation in saline aquifers. Chem Geol 265, 4453.CrossRefGoogle Scholar
Falini, G., Fermani, S. & Ripamonti, A. (2002). Crystallization of calcium carbonate salts into beta-chitin scaffold. J Inorg Biochem 91, 475480.CrossRefGoogle ScholarPubMed
Fujita, Y., Redden, G.D., Ingram, J.C., Cortez, M.M., Ferris, F.G. & Smith, R.W. (2004). Strontium incorporation into calcite generated by bacterial ureolysis. Geochim Cosmochim Acta 68, 32613270.Google Scholar
González-Muñoz, M.T., Rodriguez-Navarro, C., Martınez-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, 3150. Geological Society of London.Google Scholar
Hammersley, A.P. & Riekel, C. (1989). MFIT: Multiple spectra fitting program. Synchrotron Radiation News 2, 2426.Google Scholar
Hirschler, A., Lucas, J. & Hubert, J.-C. (1990). Bacterial involvement in apatite genesis. FEMS Microbiol Lett 73, 211220.CrossRefGoogle Scholar
House, W.A. (1987). Inhibition calcite crystal growth by inorganic phosphate. J Colloid Interface Sci 119, 505511.Google Scholar
Jones, B. (2010). Microbes in caves: Agents of calcite corrosion and precipitation. In Tufas and Speleothems: Unravelling the Microbial and Physical Controls, Pedley, H.M. & Rogerson, M. (Eds.), pp. 730. London: Geological Society, Special Publications.Google Scholar
Katsifaras, A. & Spanis, N. (1999). Effect of inorganic phosphate ions on the spontaneous precipitation of vaterite and on the transformation of vaterite in calcite. J Cryst Growth 204, 183190.Google Scholar
Kontrec, J., Kralj, D., Brecevic, L. & Falini, G. (2008). Influence of some polysaccharides on the production of calcium carbonate filler particles. J Cryst Growth 310, 45544560.Google Scholar
Lin, Y.-P. & Singer, P.C. (2005). Inhibition of calcite crystal growth by polyphosphates. Water Res 39, 48354843.Google Scholar
Marvasi, M., Visscher, P.T., Perito, B., Mastromei, G. & Casillas-Martínez, L. (2010). Physiological requirements for carbonate precipitation during biofilm development of Bacillus subtilis etfA mutant. FEMS Microbiol Ecol 71, 341350.Google Scholar
Obst, M., Dynes, J.J., Lawrence, J.R., Swerhone, G.D.W., Benzerara, K., Karunakaran, C., Kaznatcheev, K., Tyliszczak, T. & Hitchcock, A.P. (2009). Precipitation of amorphous CaCO3 (aragonite-like) by cyanobacteria: A STXM study of the influence of EPS on the nucleation process. Geochim Cosmochim Acta 73, 41804198.Google Scholar
Oelkers, E.H., Golubev, S.V., Pokrovsky, O.S. & Bénézeth, P. (2011). Do organic ligands affect calcite dissolution rates? Geochim Cosmochim Acta 75, 17991813.CrossRefGoogle Scholar
Ogino, T., Suzuki, T. & Sawada, K. (1990). The rate and mechanism of polymorphic transformation of calcium carbonate in water. J Cryst Growth 100, 159167.Google Scholar
Peckmann, J.R., Thiel, V., Reitner, J., Taviani, M., Aharon, P. & Michaelis, W. (2004). A microbial mat of a large sulfur bacterium preserved in a miocene methane-seep limestone. Geomicrobiol J 21, 247255.Google Scholar
Portillo, M. & Gonzalez, J. (2009). Comparing bacterial community fingerprints from white colonizations in Altamira cave (Spain). World J Microbiol Biotechnol 25, 13471352.Google Scholar
Portillo, M.C. & Gonzalez, J.M. (2011). Moonmilk deposits originate from specific bacterial communities in Altamira cave (Spain). Microb Ecol 61, 182189.CrossRefGoogle ScholarPubMed
Reiche, I. & Chalmin, E. (2009). Calcite formation on cave art dating back to the upper Paleolithic: The example of the Large cave of Arcy-sur-cure (28,000–24,500 BP, Yonne, France). International Congress of Rock Art, IFRAO, National Park Serra da Capivara, Piaui, Brazil. Google 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, 277287.Google Scholar
Rodriguez-Navarro, C., Jimenez-Lopez, C., Rodriguez-Navarro, A., Gonzalez-Munoz, M.T. & Rodriguez-Gallego, M. (2007). Bacterially mediated mineralization of vaterite. Geochim Cosmochim Acta 71, 11971213.CrossRefGoogle Scholar
Rooney, D.C., Hutchens, E., Clipson, N., Bladini, J. & McDermott, F. (2010). Microbial community diversity of moonmilk deposits at Ballynamintra cave, Co. Waterford, Ireland. Microb Ecol 60, 753761.Google Scholar
Rusznyak, A., Akob, D.M., Nietzsche, S., Eusterhues, K., Totsche, K.U., Neu, T.R., Frosch, T., Popp, J., Keiner, R., Geletneky, J., Katzschmann, L., Schulze, E.-D. & Küsel, K. (2012). Calcite biomineralization by bacterial isolates from the recently discovered pristine karstic Herrenberg cave. Appl Environ Microbiol 78, 11571167.CrossRefGoogle ScholarPubMed
Sanchez-Moral, S., Canaveras, J.C., Laiz, L., Saiz-Jimenez, C., Bedoya, J. & Luque, L. (2003). Biomediated precipitation of calcium carbonate metastable phases in hypogean environments: A short review. Geomicrobiol J 20, 491500.Google Scholar
Schabereiter-Gurtner, C., Saiz-Jimenez, C., Piñar, G., Lubitz, W. & Rölleke, S. (2002). Altamira cave Paleolithic paintings harbor partly unknown bacterial communities. FEMS Microbiol Lett 211, 711.CrossRefGoogle ScholarPubMed
Schmittner, K.-E. & Giresse, P. (1999). Micro-environmental controls on biomineralization: Superficial processes of apatite and calcite precipitation in quaternary soils, Roussillon, France. Sedimentology 46, 463476.Google Scholar
Schultze-Lam, S., Fortin, D., Davis, B.S. & Beveridge, T.J. (1996). Mineralization of bacterial surfaces. Chem Geol 132, 171181.Google Scholar
Schultze-Lam, S., Harauz, G. & Beveridge, T.J. (1992). Participation of cyanobacterial S layer in fine-grain mineral formation. J Bacteriol 174, 79717981.Google Scholar
Solé, V.A., Papillon, E., Cotte, M., Walter, P. & Susini, J. (2007). A multiplatform code for the analysis of energy-dispersive X-ray fluorescence spectra. Spectrochim Acta B 62, 6368.CrossRefGoogle Scholar
Somogyi, A., Drakopoulos, M., Vincze, L., Vekemans, B., Camerani, C., Janssens, K., Snigirev, A. & Adams, F. (2001). ID18F: A new micro-X-ray fluorescence end-station at the European Synchrotron Radiation Facility (ESRF): Preliminary results. X-ray Spectrom 30, 242252.Google Scholar
Souza-Egipsy, V., García Del Cura, M.A., Ascaso, C., De Los Ríos, A., Wierzchos, J. & González-Martín, J.A. (2006). Interaction between calcite and phosphorus in biomineralization processes in tufa carbonates. Int Rev Hydrobiol 91, 222241.Google Scholar
Spötl, C., Fairchild, I.J. & Tooth, A.F. (2005). Cave air control geochemistry, Obir caves (Austria): Implications for speleothem deposition in dynamically ventilated caves. Geochim et Cosmochim Acta 69, 24512468.Google Scholar
Susini, J., Salomé, M., Fayard, B., Ortega, R. & Kaulich, B. (2002). The scanning X-ray microprobe at the ESRF “X-ray microscopy” beamline. Surf Rev Lett 9, 203211.CrossRefGoogle Scholar
Tourney, J. & Ngwenya, B.T. (2009). Bacterial extracellular polymeric substances (EPS) mediate CaCO3 morphology and polymorphism. Chem Geol 262, 138146.Google Scholar
Tröger, L., Arvanitis, D., Baberschke, K., Michaelis, H., Grimm, U. & Zschech, E. (1992). Full correction of the self-absorption in soft-fluorescence extended X-ray-absorption fine structure. Phys Rev B 46, 32833289.Google Scholar
White, W.B. (2003). Paleoclimate records from speleothems in limestone caves. In Studies of Cave Sediment. Physical and Chemical Records of Paleoclimate, Sasowsky, I.D. & Mylroie, J. (Eds.), pp. 135175. New York: Kluwer Academic/Plenum.Google Scholar
Zimmermann, J., Gonzalez, J.M., Saiz-Jimenez, C. & Ludwig, W. (2005). Detection and phylogenetic relationships of highly diverse uncultured acidobacterial communities in Altamira cave using 23S rRNA sequence analyses. Geomicrobiol J 22, 379388.Google Scholar
Supplementary material: PDF

Chalmin Supplementary Material

Figure

Download Chalmin Supplementary Material(PDF)
PDF 152.2 KB