Penelope J. Boston

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.

Life in Earth’s Lava Caves: Implications for Life Detection on Other Planets

Lava caves represent a scientifically untapped habitat in which to study Earth’s microbial life and provide an outstanding environment in which to identify biosignatures for detecting life on other planets. Our studies of microbial mats and mineral deposits in lava caves in the Azores (Portugal), New Mexico, and Hawai‘i (USA) have revealed a wealth of bacterial diversity through molecular genetic analyses and scanning electron microscopy. Much of this bacterial diversity represents novel species, as well as novel higher taxonomic units, such as genera and families. Geochemical analyses of infiltrating water, soils, and rock walls suggest the presence of organic carbon that may fuel heterotrophy and reduce inorganic energy sources, such as iron, manganese, and sulfur to fuel chemolithotrophy. Scanning electron microscopy studies of mineral deposits, accompanied by molecular studies, reveals the presence of extensive biological morphologies in a variety of mineral deposits decorating lava cave walls. These studies provide a rationale for examining mineral deposits in lava caves on extraterrestrial bodies in the search for life or its remnants.