Abstract
The influence of bacterial communities on the formation of carbonate deposits such as moonmilk was investigated in Altamira Cave (Spain). The study focuses on the relationship between the bacterial communities at moonmilk deposits and those forming white colonizations, which develop sporadically throughout the cave. Using molecular fingerprinting of the metabolically active bacterial communities detected through RNA analyses, the development of white colonizations and moonmilk deposits showed similar bacterial profiles. White colonizations were able to raise the pH as a result of their metabolism (reaching in situ pH values above 8.5), which was proportional to the nutrient supply. Bacterial activity was analyzed by nanorespirometry showing higher metabolic activity from bacterial colonizations than uncolonized areas. Once carbonate deposits were formed, bacterial activity decreased drastically (down to 5.7% of the white colonization activity). This study reports on a specific type of bacterial community leading to moonmilk deposit formation in a cave environment as a result of bacterial metabolism. The consequence of this process is a macroscopic phenomenon of visible carbonate depositions and accumulation in cave environments.
Similar content being viewed by others
References
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Barton HA, Northup DE (2007) Geomicrobiology in cave environments: past, current and future perspectives. J Cave Karst Stud 69:163–178
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
Braissant O, Verrecchia EP, Aragno M (2002) Is the contribution of bacteria to terrestrial carbon budget greatly underestimated? Naturwissenschaften 89:366–370
Bruce JP, Frome M, Haites E, Janzen H, Lal R, Paustian K (1999) Carbon sequestration in soil. J Soil Water Conserv 54:382–389
Butler JN (1982) Carbon dioxide equilibria and their applications. Addison-Wesley, Reading, 259pp
Callot G, Mousain D, Plassard C (1985) Concentrations de carbonate de calcium sur les parois del hyphes mycéliens. Agronomie 5:143–150
Cañaveras JC, Sanchez-Moral S, Soler V, Saiz-Jimenez C (2001) Microorganisms and microbially induced fabrics in cave walls. Geomicrobiol J 18:223–240
Cañaveras JC, Cuezva S, Sanchez-Moral S, Lario J, Laiz L, Gonzalez JM, Saiz-Jimenez C (2006) On the origin of fiber calcite crystals in moonmilk deposits. Naturwissenschaften 93:27–32
Castanier S, Le Metayer-Levrel G, Perthuisot J-P (1999) Ca-carbonates precipitation and limestone genesis—the microbiogeologists point of view. Sedim Geol 126:9–23
Chelius MK, Beresford G, Horton H, Quirk M, Selby G, Simpson RT, Horrocks R, Moore JC (2009) Impacts of alterations of organic inputs on the bacterial community within the sediments of Wind Cave, South Dakota, USA. Intl J Speleol 38:1–10
Crank J (1997) The mathematics of diffusion, 2nd edn. Oxford Science, Oxford
Cuezva S, Sanchez-Moral S, Saiz-Jimenez C, Cañaveras JC (2009) Microbial communities and associated mineral fabrics in Altamira Cave, Spain. Intl J Speleol 38:83–92
Curtis TP, Sloan WT, Scannell JW (2002) Estimating prokaryotic diversity and its limits. Proc Natl Acad Sci USA 99:10494–10499
Ehrlich HL (1998) Geomicrobiology: its significance for geology. Earth Sci Rev 45:45–60
Fromin N, Hamelin J, Tarnawski S, Roesti D, Jourdain-Miserez K, Forestier N, Teyssier-Cuvelle S, Gillet F, Aragno M, Rossi P (2002) Statistical analysis of denaturing gel electrophoresis (DGE) fingerprinting patterns. Environ Microbiol 4:634–643
Gonzalez JM, Ortiz-Martinez A, Gonzalez-del Valle MA, Laiz L, Saiz-Jimenez C (2003) An efficient strategy for screening large cloned libraries of amplified 16 S rDNA sequences from complex environmental communities. J Microbiol Meth 55:459–463
Gonzalez JM, Zimmermann J, Saiz-Jimenez C (2005) Evaluating putative chimeric sequences from PCR amplified products and other cross-over events. Bioinformatics 21:333–337
Gonzalez JM, Portillo MC, Saiz-Jimenez C (2006) Metabolically active Crenarchaeota in Altamira Cave. Naturwissenschaften 93:42–45
Hughes JB, Hellmann JJ (2005) The application of rarefaction techniques to molecular inventories of microbial diversity. Meth Enzymol 397:292–308
Kowalski AS, Serrano-Ortiz P, Janssens IA, Sanchez-Moral S, Cuezva S, Domingo F, Were A, Alados-Arboledas L (2008) Can flux tower research neglect geochemical CO2 exchange? Agric For Meteorol 148:1045–1054
Lasheras JA (2002) Redescubrir Altamira. Turner, Madrid, Spain
Morse JW, Mackenzie F (1990) Geochemistry of Sedimentary Carbonates. Elsevier, Maryland Heights, 696pp
Muyzer G, de Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction-amplified genes coding for 16 S rRNA. Appl Environ Microbiol 59:695–700
Nielsen P, Larsen LH, Ramlov H, Hansen BW (2007) Respiration rates of subitaneous eggs from a marine calanoid copepod: monitored by nanorespirometry. J Comp Physiol B 177:287–296
Northup DE, Lavoie KH (2001) Geomicrobiology of caves: a review. Geomicrobiol J 18:199–222
Portillo MC, Gonzalez JM (2008) Statistical differences between molecular fingerprints from microbial communities. Antonie Leeuwenhoek 94:157–163
Portillo MC, Gonzalez JM (2009) Sulfate-reducing bacteria are common members of bacterial communities in Altamira Cave (Spain). Sci Total Environ 407:1114–1122
Portillo MC, Gonzalez JM (2010) Differential effects of distinct bacterial biofilms in a cave environment. Curr Microbiol 60:435–438
Portillo MC, Gonzalez JM, Saiz-Jimenez C (2008) Metabolically active microbial communities of yellow and grey colonizations on the walls of Altamira Cave, Spain. J Appl Microbiol 104:681–691
Portillo MC, Saiz-Jimenez C, Gonzalez JM (2009) Molecular characterization of total and metabolically active bacterial communities of “white colonizations” in Altamira Cave, Spain. Res Microbiol 160:41–47
Portillo MC, Porca E, Cuezva S, Sanchez-Moral S, Gonzalez JM (2009) Is the availability of different nutrients a critical factor for the impact of bacteria on subterraneous carbon budgets? Naturwissenschaften 96:1035–1042
Revsbech NP (2005) Analysis of microbial communities with electrochemical microsensors and microscale biosensors. Meth Enzymol 397:147–166
Sanchez-Moral S, Soler V, Cañaveras JC, Sanz E, van Grieken R, Gysells K (1999) Inorganic deterioration affecting Altamira Cave. Quantitative approach to wall-corrosion (solution etching) processes induced by visitors. Sci Total Environ 243:67–84
Zimmermann J, Gonzalez JM, Ludwig W, Saiz-Jimenez C (2005) Detection and phylogenetic relationships of a highly diverse uncultured acidobacterial community on paleolithic paintings in Altamira Cave using 23 S rRNA sequence analyses. Geomicrobiol J 22:379–388
Acknowledgements
The authors acknowledge support through project CGL2006-11561/BTE from the Spanish Ministry of Education and Science. All Altamira Cave Research Centre and Museum staff are acknowledged for facilitating this research.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Portillo, M.C., Gonzalez, J.M. Moonmilk Deposits Originate from Specific Bacterial Communities in Altamira Cave (Spain). Microb Ecol 61, 182–189 (2011). https://doi.org/10.1007/s00248-010-9731-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-010-9731-5