Microbial communities in a coastal cave: Cova des Pas de Vallgornera (Mallorca, Western Mediterranean)

International Journal of Speleology

Volumn 43, Issue 2, 2014, Pages 205-216

  Busquets, Antoni ^a   Fornós, Joan J ^a   Zafra, Freddy ^a   Lalucat, Jorge ^a,b   Merino, Antoni ^c  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b INSTITUTO MEDITERRÁNEO DE ESTUDIOS AVANZADOS   (Spain)

^c IMEDEA ^*  (Spain)

Author keywords

Anchialine; Brackish pools; Carbonate precipitates; Ferromanganese deposits; Fungi; Littoral cave; Mallorca; Microbial community

Indexed keywords

BIOGEOCHEMISTRY; CALCITE; CARBONATE ROCK; CAVE; COASTAL ZONE; FERROMANGANESE DEPOSIT; FUNGUS; KARST; LITTORAL ENVIRONMENT; MICROBIAL COMMUNITY; SPECIES DIVERSITY;

BALEARIC ISLANDS; MAJORCA; MEDITERRANEAN SEA; SPAIN;

ACTINOBACTERIA; ASPERGILLUS; BACTERIA (MICROORGANISMS); FUNGI; GAMMAPROTEOBACTERIA; NOCARDIOIDES LUTEUS; PSEUDOMONAS;

EID: 84902127703     PISSN: 03926672     EISSN: 1827806X     Source Type: Journal    
DOI: 10.5038/1827-806X.43.2.8     Document Type: Article

References (67)

1. Aloisi G., Gloter A., Krüger M., Wallmann K., Guyot F. & Zuddas P., 2006. Nucleation of calcium carbonate on bacterial nanoglobules. Geology, 34: 1017-1020. http://dx.doi.org/10.1130/G22986A.1
2. Amann R.I., Binder B.J., Olson R.J., Chisholm S.W., Devereux R. & Stahl D.A., 1990. Combination of 16S rRNA-Targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Applied and Environmental Microbiology, 56 (6): 1919-1925.
3. Banks E.D., Taylor N.M., Gulley J., Lubbers B.R., Giarrizo J.G., Bullen H.A., Hoehler T.M. & Barton H.A., 2010. Bacterial calcium carbonate precipitation in cave environments: a function of calcium homeostasis. Geomicrobiology Journal, 27: 444-454. http://dx.doi.org/10.1080/01490450903485136
4. Barrón C. & Duarte C.M., 2009. Dissolved organic matter release in a Posidonia oceanica meadow. Marine Ecology Progress Series, 374: 75-84. http://dx.doi.org/10.3354/meps07715
5. Barton H.A. & Northup D.E., 2007. Geomicrobiology in cave environments: past, current and future perspectives. Journal of Cave and Karst Studies, 69 (1): 163-178.
6. 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. http://dx.doi.org/10.1038/246527a0
7. Bosak T., Souza-Egipsy V. & Newman K., 2004. A laboratory model for abiotic peloid formation. Geobiology, 2: 189-198. http://dx.doi.org/10.1111/j.1472-4677.2004.00031.x
8. Cacchio P., Contento R., Ercole C., Cappuccio G., Martinez M.P. & Lepidi A., 2004. Involvement of microorganisms in the formation of carbonate speleothems in the Cervo Cave (L'Aquila-Italy). Geomicrobiology Journal, 21: 497-509. http://dx.doi.org/10.1080/01490450490888109
9. 3 in orthox soils of Biga, Ivory Coast. Catena, 59: 1-17. http://dx.doi.org/10.1016/j.catena.2004.06.002
10. Castanier S., Le Métayer-Levrel G. & Perthuisot J.P., 1999. Ca-carbonate precipitation and limestone genesis-the microbiologist point of view. Sedimentary Geology, 126: 9-23. http://dx.doi.org/10.1016/S0037-0738(99)00028-7
11. Daims H., Brühl A., Amann R., Schleifer K.H. & Wagner M., 1999. The domain-specific probe EUB338 is insufficient for the detection of all Bacteria: development and evaluation of a more comprehensive probe set. Systematic and Applied Microbiology, 22: 434-444. http://dx.doi.org/10.1016/S0723-2020(99)80053-8
12. Dorale J.A., Onac B.P., Fornós J.J., Ginés J., Ginés A., Tuccimei P. & Peate D.W., 2010. Sea-level 81,000 years ago in Mallorca. Science, 327: 860-863. http://dx.doi.org/10.1126/science.1181725
13. Dupraz C., Visscher P.T., Baumgartner L.K. & Reid R.P., 2004. Microbe-mineral interactions: early carbonate precipitation in a hypersaline lake (Eleuthera Island, Bahamas). Sedimentology, 51: 745-765. http://dx.doi.org/10.1111/j.1365-3091.2004.00649.x
14. th ed.) New York: Marcel Dekker, Inc. Fairchild I.J. & Baker A., 2012. Speleothem science. From process to past environments. Wiley Blackwell. http://dx.doi.org/10.1002/9781444361094
15. Felsenstein J., 1989. PHYLIP-phylogeny inference package (version 3.0). Cladistics, 5: 164-166.
16. Fernández-Díaz L., Putnis A., Prieto M. & Putnis C.V., 1996. The role of magnesium in the crystallization of calcite and aragonite in a porous medium. Journal of Sedimentary Research, 66: 482-491.
17. Fornós J.J., Merino A., Ginés J., Ginés A. & Gràcia F., 2011. Solutional features and cave deposits related to hypogenespeleogenetic processes in a littoral cave of Mallorca Island (western Mediterranean). Carbonates and Evaporites, 26 (1): 69-81. http://dx.doi.org/10.1007/s13146-010-0040-3
18. Fornós J.J., Pomar L. & Ramos Guerrero E., 2002. Balearic Islands. In: Gibbons W. & Moreno T. (Eds.), The Geology of Spain. London: The Geological Society: 327-334.
19. Ginés A. & Ginés J., 1986. On the interest of speleochronological studies in karstified islands. The case of Mallorca (Spain). Proceedings of the 9th International Congress of Speleology, Barcelona, 1: 297-300.
20. Ginés A., Ginés J., Gómez-Pujol L., Onac B.P. & Fornós J.J. (Eds.), 2012. Mallorca: a Mediterranean benchmark for Quaternary studies. Monografies de la Societat d'Història Natural de les Balears, 18. Palma de Mallorca, 219 p.
21. th International Congress of Speleology. Kerville: National Speleological Society, 1: 481-487.
22. Ginés J., Ginés A., Fornós J.J., Merino A. & Gràcia F., 2009b. On the role of hypogene speleogenesis in shaping the coastal endokarst of southern Mallorca (western Mediterranean). In: Klimchouk A.B. & Ford D.C. (Eds.), Hypogene speleogenesis and karst hydrogeology of artesian basins. Ukrainian Institute of Speleology and Karstology, Special Paper 1, Simferopol, Ukraine: 91-99.
23. Ginés J., Fornós J.J., Ginés A., Merino A. & Gràcia F., 2014. Geologic constraints and speleogenesis of Cova des Pas de Vallgornera, a complex coastal cave from Mallorca Island (Western Mediterranean). International Journal of Speleology, 43 (1): 105-124 http://dx.doi.org/10.5038/1827-806X.43.2.2
24. Gomila M., Gascó J., Busquets A., Gil J., Bernabeu R., Buades J.M. & Lalucat J., 2005. Identification of culturable bacteria present in haemodialysis water and fluid. FEMS Microbiology Ecology, 52: 101-114. http://dx.doi.org/10.1016/j.femsec.2004.10.015
25. Gonzalez B.C., Iliffe T.M., Macalady J.L., Schaperdoth I. & Kakuk B., 2011. Microbial hotspots in anchialine blueholes: initial discoveries from the Bahamas. Hydrobiologia, 677: 149-156. http://dx.doi.org/10.1007/s10750-011-0932-9
26. Gràcia F., Fornós J.J., Clamor B., Febrer M. & Gamundí, P., 2007. La cova de sa Gleda I. Sector Clàssic, Sector de Ponent i Sector Cinc-cents. (Manacor, Mallorca): Geomorfologia, espeleogènesi, sedimentologia i hidrología. Endins, 31: 43-96.
27. Gràcia F., Fornós J.J., Gamundí P., Clamor B., Pocoví J. & Perelló M.A., 2009. Les descobertes subaqaàtiques a la Cova des Pas de Vallgornera (llucmajor, Mallorca): Història i descripció dels descobriments, hidrologia, espeleotemes, sediments, paleontología i fauna. Endins, 33: 35-72.
28. Gràcia F., Ginés J., Pons G.X., Ginard A. & Vicens D. (Eds.), 2011. El carst, patrimoni natural de les Illes Balears. Endins, 35 / Monografies de la Societat d'Història Natural de les Balears, 17, 368 p.
29. Gray C.J. & Engel A.S., 2013. Microbial diversity and impact on carbonate geochemistry across a changing geochemical gradient in a karst aquifer. The ISME Journal, 7: 325-337. http://dx.doi.org/10.1038/ismej.2012.105
30. Jones B., 2010. Microbes in caves: agents of calcite corrosion and precipitation. In: Pedley H.M. & Rogerson M. (Eds.), Tufas and speleothems: Unravelling the microbial and physical controls. Geological Society, London, Special Publication, 336: 7-30.
31. Jukes T.H. & Cantor C.R., 1969. Evolution of protein molecules. In: Munro H.N. (Ed.), Mammalian protein metabolism. New York: Academic Press: 21-132. http://dx.doi.org/10.1016/B978-1-4832-3211-9.50009-7
32. Kemp P.F. & Aller J.Y., 2004. Estimating prokaryotic diversity: when are 16S rDNA libraries large enough? Limnology and Oceanography Methods, 2: 114-125. http://dx.doi.org/10.4319/lom.2004.2.114
33. Krstulović N., Šolić M., Šantić D., Maršić-Lucić J., Ordulf M. & Šestanović S., 2013. Microbial community structure in two anchialine caves on Mljet Island (Adriatic Sea). Acta Adriatica, 54 (2): 183-198.
34. Lace M.J. & Mylroie J.E. (Eds.), 2013. Coastal karst landforms. Coastal Research Library, 5. Springer, Berlin. http://dx.doi.org/10.1007/978-94-007-5016-6
35. Lane D.J., 1991. 16S/23S rRNA sequencing. In: Stackebrandt E. & Goodfellow M. (Eds.), Nucleic acid techniques in bacterial systematics. John Wiley & Sons, 115-175.
36. Manz W., Amann R., Ludwig W., Wagner M. & Schleifer K.H., 1992. Phylogenetic oligodeoxynucleotide probes for the major subclasses of proteobacteria: problems and solutions. Systematic and Applied Microbiology, 15: 593-600. http://dx.doi.org/10.1016/S0723-2020(11)80121-9
37. Medlin L., Elwood H.J., Stickel S. & Sogin M.L., 1988. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene, 71: 491-499. http://dx.doi.org/10.1016/0378-1119(88)90066-2
38. Melim L.A., Liescheidt R., Northup D.E., Spilde M.N., Boston P.J. & Queen J.M., 2009. A biosignature suite from cave pool precipitates, Cottonwood Cave, New Mexico. Astrobiology, 9 (9): 907-917. http://dx.doi.org/10.1089/ast.2009.0345
39. th International Congress of Speleology. Kerrville: National Speleological Society, 1: 307-311.
40. Merino A., Fornós J.J. & Ginés A., 2011a. Espeleotemes i minerals de les coves de Mallorca. In: Gràcia F., Ginés J., Pons G.X., Ginard A. & Vicens, D. (Eds.), El carst, patrimoni natural de les Illes Balears. Endins, 35 / Monografies de la SocIetat d'Història Natural de les Balears, 17:183-198.
41. Merino A., Mulet A., Mulet G., Croix A., Kristofersson A., Gràcia F. & Perelló M.A., 2014a. History and description of Cova des Pas de Vallgornera, (Mallorca, Spain): history of exploration and cave description. International Journal of Speleology, 43 (2): 95-104. http://dx.doi.org/10.5038/1827-806X.43.2.1
42. Merino A., Mulet A., Mulet G., Croix A., Kristofersson A., Gràcia F., Ginés J. & Fornós J.J., 2011b. La Cova des Pas de Vallgornera (Llucmajor, Mallorca). La cova de major desenvolupament de les Illes Balears. Endins, 35 / Monografies de la Societat d'Història Natural de les Balears, 17: 147-164.
43. Merino A., Ginés J., Tuccimei P., Soligo M. &, Fornós J.J., 2014b. Speleothems in Cova des Pas de Vallgornera: their distribution and characteristics within an extensive coastal cave from the eogenetic karst of southern Mallorca (Western Mediterranean). International Journal of Speleology, 43 (2): 125-142. http://dx.doi.org/10.5038/1827-806X.43.2.3
44. Northup D.E., Barns S.M., Yu L.E., Spilde M.N., Schelble R.L.T., Dano K.E., Crossey L.J., Connolly C.A., Boston P.J., Natvig D.O. & Dahm C.N. 2003. Diverse microbial communities inhabiting ferromanganese deposits in Lechuguilla and Spider caves. Environmental Microbiology, 5:1071-1086.
45. Northup D.E. & Lavoie K.H., 2001. Geomicrobiology of caves: a review. Geomicrobiology Journal, 18: 199-222. http://dx.doi.org/10.1080/01490450152467750
46. Onac B.P., Fornós J.J., Merino A., Ginés J. & Diehl J., 2014. Linking mineral deposits to speleogenetic processes in Cova des Pas de Vallgornera (Mallorca, Spain). International Journal of Speleology, 43 (2): 143-157. http://dx.doi.org/10.5038/1827-806X.43.2.4
47. Page R.D.M., 1996. TREEVIEW: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12: 357-358.
48. Pasic L., Kovce B., Sket B. & Herzog-Velikonja B., 2010. Diversity of microbial communities colonizing the walls of a karstic cave in Slovenia. FEMS Microbiology Ecology, 71: 50-60. http://dx.doi.org/10.1111/j.1574-6941.2009.00789.x
49. Pomar L., 1991. Reef geometries, erosion surfaces and high-frequency sea-level changes, upper Miocene Reef Complex, Mallorca, Spain. Sedimentology, 38: 243-269. http://dx.doi.org/10.1111/j.1365-3091.1991.tb01259.x
50. Pomar L., Ward W.C. & Grenn D.G., 1996. Upper Miocene reef. Complex of the Llucmajor area, Mallorca, Spain. In:
51. Franseen E., Esteban M., Ward, W.C. & Rouchy J.M. (Eds.), Models for carbonate stratigraphy from Miocene reef complexes of the Mediterranean regions. SEPM Concepts in Sedimentology and Paleontology, 5: 191-225.
52. Porter K. & Feig Y., 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography, 25: 943-948. http://dx.doi.org/10.4319/lo.1980.25.5.0943
53. Reasoner D.J. & Geldreich E.E. 1985. A new medium for the enumeration and subculture of bacteria from potable water. Applied Environmental Microbiology, 49: 1-7.
54. 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 Microbiology Ecology, 48: 39-46. http://dx.doi.org/10.1016/j.femsec.2003.12.008
55. Sánchez-Navas A. & Martín-Algarra A., 2001. Genesis of apatite in phosphate stromatolites. European Journal of Mineralogy, 13: 361-376. http://dx.doi.org/10.1127/0935-1221/01/0013-0361
56. Shabarova T. & Pernthaler J., 2010. Karst pools in subsurface environments: collectors of microbial diversity or temporary residence between habitat types. Environmental Microbiology, 14: 1061-1074. http://dx.doi.org/10.1111/j.1462-2920.2009.02151.x
57. Schabereiter-Gurtner C., Saiz-Jimenez C., Piñar G., Lubitz W. & Rölleke S., 2004. Phylogenetic diversity of bacteria associated with Paleolithic paintings and surrounding rock walls in two Spanish caves (Llonín and La Garma). FEMS Microbiology Ecology, 47: 235-247. http://dx.doi.org/10.1016/S0168-6496(03)00280-0
58. Seymour J.R., Humpherys W.F. & Mitchell, J.G., 2007. Stratification of the microbial community inhabiting an anchialine sinkhole. Aquatic Microbial Ecology, 50: 11-24. http://dx.doi.org/10.3354/ame01153
59. Sket B., 2005. Anchialine caves. In: Culver D.C. & White W.B. (Eds.)-Encyclopedia of Caves. Elsevier Academic Press: 30-37.
60. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F. & Higgins D.G., 1997. The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research, 25: 4876-4882. http://dx.doi.org/10.1093/nar/25.24.4876
61. Tuccimei P., Ginés J., Delitala M.C., Ginés A., Gràcia F., Fornós J.J. & Taddeucci, A., 2006. Last interglacial sea level changes in Mallorca Island (western Mediterranean). High precision U-series data from phreatic overgrowths on speleothems. Zeitschrift für Geomorphologie, 50 (1): 1-21.
62. Tucker M.E. & Wright V.P., 1990. Carbonate sedimentology. Blackwell. http://dx.doi.org/10.1002/9781444314175
63. Van Lith Y., Warthmann R., Vasconcelos C. & McKenzie J., 2003. Microbial fossilization in carbonate sediments: a result of the bacterial surface involvement in dolomite precipitation. Sedimentology, 50: 237-245. http://dx.doi.org/10.1046/j.1365-3091.2003.00550.x
64. Van Lith Y., Warthmann R., Vasconcelos C. & McKenzie J.A., 2003. Sulphate-reducing bacteria and dolomite/ calcite formation sulphate-reducing bacteria induce lowtemperature Ca-dolomite and high Mg-calcite formation. Geobiology, 1: 71-79. http://dx.doi.org/10.1046/j.1472-4669.2003.00003.x
65. Wilson K., 1987. Preparation of genomic DNA from bacteria. In: Ausubel F. M., Brent R., Kingston R. E., Moore D. D., Seidman J. G., Smith J. A. & Struhl K. (Eds.), Current protocols in molecular biology. John Wiley & Sons, New York: 241-242.
66. Wilson W.L. & Morris T.L., 1994. Cenote Verde: a meromictic karst pond, Quintana Roo, Mexico. In: Sasowsky I. D, Palmer M. V, (Eds.). Breakthroughs in karst geomicrobiology and redox geochemistry: Abstracts and field-trip guide for the symposium held February 16 through 19, 1994, Colorado Springs, Colorado. Charles Town, WV: Karst Waters Institute: Special Publication 1: 77-79.
67. Welker M. & Moore E.R.B., 2011. Applications of wholecell matrix-assisted laser-desorption/ionization timeof-flight mass spectrometry in systematic microbiology. Systematic and Applied Microbiology, 34: 2-11. http://dx.doi.org/10.1016/j.syapm.2010.11.013