Microbiology and geochemistry in a hydrogen-sulphide-rich karst environment

Abstract Cueva de Villa Luz, a hypogenic cave in Tabasco, Mexico, offers a remarkable opportunity to observe chemotrophic microbial interactions within a karst environment. The cave water and atmosphere are both rich in hydrogen sulphide. Measured H 2 S levels in the cave atmosphere reach 210 ppm, and SO 2 commonly exceeds 35 ppm. These gases, plus oxygen from the cave air, are absorbed by freshwater that accumulates on cave walls from infiltration and condensation. Oxidation of sulphur and hydrogen sulphide forms concentrated sulphuric acid. Drip waters contain mean pH values of 1.4, with minimum values as low as 0.1. The cave is fed by at least 26 groundwater inlets with a combined flow of 200–300 l/s. Inlet waters fall into two categories: those with high H 2 S content (300–500 mg/l), mean P CO 2 =0.03–0.1 atm, and no measurable O 2 ; and those with less than 0.1 mg/l H 2 S, mean P CO 2 =0.02 atm, and modest O 2 content (up to 4.3 mg/l). Both water types have a similar source, as shown by their dissolved solid content. However, the oxygenated water has been exposed to aerated conditions upstream from the inlets so that original H 2 S has been largely lost due to outgassing and oxidation to sulphate, increasing the sulphate concentration by about 4%. Chemical modelling of the water shows that it can be produced by the dissolution of common sulphate, carbonate, and chloride minerals. Redox reactions in the cave appear to be microbially mediated. Sequence analysis of small subunit (16 S ) ribosomal RNA genes of 19 bacterial clones from microbial colonies associated with water drips revealed that 18 were most similar to three Thiobacilli spp., a genus that often obtains its energy from the oxidation of sulphur compounds. The other clone was most similar to Acidimicrobium ferrooxidans , a moderately thermophilic, mineral-sulphide-oxidizing bacterium. Oxidation of hydrogen sulphide to sulphuric acid, and hence the cave enlargement, is probably enhanced by these bacteria. Two cave-enlarging processes were identified. (1) Sulphuric acid derived from oxidation of the hydrogen sulphide converts subaerial limestone surfaces to gypsum. The gypsum falls into the cave stream and is dissolved. (2) Strongly acidic droplets form on the gypsum and on microbial filaments, dissolving limestone where they drip onto the cave floors. The source of the H 2 S in the spring waters has not been positively identified. The Villahermosa petroleum basin within 50 km to the northwest, or the El Chichon volcano ~50 km to the west, may serve as source areas for the rising water. Depletion of 34 S values (−11.7‰ for sulphur stabilized from H 2 S in the cave atmosphere), along with the hydrochemistry of the spring waters, favour a basinal source.

[1]  R. Raiswell Thermodynamic Values at Low Temperature for Natural Inorganic Materials: An Uncritical Summary , 1988, Mineralogical Magazine.

[2]  N. Pace,et al.  Phylogenetic analysis of the hyperthermophilic pink filament community in Octopus Spring, Yellowstone National Park , 1994, Applied and environmental microbiology.

[3]  W. Liesack,et al.  Elemental Sulfur and Thiosulfate Disproportionation by Desulfocapsa sulfoexigens sp. nov., a New Anaerobic Bacterium Isolated from Marine Surface Sediment , 1998, Applied and Environmental Microbiology.

[4]  D. Johnson,et al.  Heterotrophic Acidophiles and Their Roles in the Bioleaching of Sulfide Minerals , 1997 .

[5]  S. Waksman,et al.  MICROÖRGANISMS CONCERNED IN THE OXIDATION OF SULFUR IN THE SOIL II. THIOBACILLUS THIOOXIDANS, A NEW SULFUR-OXIDIZING ORGANISM ISOLATED FROM THE SOIL , 1922, Journal of bacteriology.

[6]  L. Hose,et al.  CUEVA DE VILLA LUZ, TABASCO, MEXICO: RECONNAISSANCE STUDY OF AN ACTIVE SULFUR SPRING CAVE AND ECOSYSTEM , 1999 .

[7]  Thomas D. Brock,et al.  Biology of microorganisms , 1970 .

[8]  E. S. Bastin,et al.  THE PRESENCE OF SULPHATE REDUCING BACTERIA IN OIL FIELD WATERS. , 1926, Science.

[9]  B L Maidak,et al.  The RDP-II (Ribosomal Database Project) , 2001, Nucleic Acids Res..

[10]  T. C. Kane,et al.  A Chemoautotrophically Based Cave Ecosystem , 1996, Science.

[11]  K. Nagy,et al.  Validation of the HTO-18 method for determination of CO/sub 2/ production of lizards (genus Sceloporus) , 1978 .

[12]  Carol A. Hill,et al.  Cave Minerals of the World , 1976 .

[13]  S. Giovannoni,et al.  Phylogenetic analysis of a natural marine bacterioplankton population by rRNA gene cloning and sequencing , 1991, Applied and environmental microbiology.

[14]  N. Pace,et al.  Remarkable archaeal diversity detected in a Yellowstone National Park hot spring environment. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[15]  A R Colmer,et al.  The Role of Microorganisms in Acid Mine Drainage: A Preliminary Report. , 1947, Science.

[16]  A. P. Harrison The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. , 1984, Annual review of microbiology.

[17]  R. Garrels,et al.  Thermodynamic values at low temperature for natural inorganic matericals : an uncritical summary , 1987 .

[18]  A. Palmer Origin and morphology of limestone caves , 1991 .

[19]  P. Dugan,et al.  Aerobic Heterotrophic Bacteria Indigenous to pH 2.8 Acid Mine Water: Microscopic Examination of Acid Streamers , 1970, Journal of bacteriology.

[20]  Douglas E. Rawlings,et al.  Biomining : Theory, Microbes and Industrial Processes , 2006 .

[21]  C. Kuske,et al.  Diverse uncultivated bacterial groups from soils of the arid southwestern United States that are present in many geographic regions , 1997, Applied and environmental microbiology.

[22]  A. Palmer Geochemical Models for the Origin of Macroscopic Solution Porosity in Carbonate Rocks , 1995 .

[23]  David B. Ringelberg,et al.  Changes in Bacteria Recoverable from Subsurface Volcanic Rock Samples during Storage at 4°C , 1994 .

[24]  G J Olsen,et al.  Evolutionary relationships among sulfur- and iron-oxidizing eubacteria , 1992, Journal of bacteriology.

[25]  J. L. Macías,et al.  Geochemistry of the volcano-hydrothermal system of El Chichón Volcano, Chiapas, Mexico , 1998 .

[26]  M. Menichetti,et al.  Occurrence of hypogenic caves in a karst region: Examples from central Italy , 1995 .

[27]  E. Busenberg,et al.  The kinetics of dissolution of dolomite in CO 2 -H 2 O systems at 1.5 to 65 degrees C and O to 1 atm PCO 2 , 1982 .

[28]  G. Bitton,et al.  Biogeochemical ecology of Thiothrix spp. In underwater limestone caves , 1994 .

[29]  A common pathway of sulfide oxidation by sulfate‐reducing bacteria , 1996 .

[30]  D. Langmuir,et al.  The geochemistry of some carbonate ground waters in central Pennsylvania , 1971 .

[31]  T. Casadevall,et al.  Crater lake and post-eruption hydrothermal activity, El Chichón Volcano, Mexico , 1984 .

[32]  D. Kushner Microbial life in extreme environments , 1980 .

[33]  B. Jørgensen The sulfur cycle of freshwater sediments: Role of thiosulfate , 1990 .

[34]  D. Canfield,et al.  The production of 34S-depleted sulfide during bacterial disproportionation of elemental sulfur. , 1994, Science.

[35]  D. Canfield,et al.  Isotope fractionation and sulfur metabolism by pure and enrichment cultures of elemental sulfur‐disproportionating bacteria , 1998 .

[36]  D. Rosen,et al.  A Cavernicolous Form of the Poeciliid Fish Poecilia sphenops from Tabasco, Mexico , 1962 .