Chemolithoautotrophy in a shallow-sea hydrothermal system, Milos Island, Greece

In recent decades, numerous (hyper)thermophilic microorganisms have been isolated from hydrothermal venting systems. Although they have been shown to have the capabilities to catalyze a wide variety of reactions to gain energy, few pure cultures have been isolated from these environments. In order to more fully understand the catabolic potential of organisms living in and near hydrothermal vents, we have calculated the Gibbs energies (ΔGr) of 730 redox reactions that could be supplying energy to organisms in the shallow-sea hydrothermal sediments of Paleochori Bay, Milos Island, Greece. This analysis required in-depth geochemical data on the pore fluids and minerals in these sediments near the vent site at several depths. The geochemical profiles of Saganaki vent show steep gradients in temperature, pH, and redox-sensitive compounds resulting from the mixing of hot ( 75oC), acidic ( pH 4), chemically reduced venting fluid with colder, slightly basic and oxidized seawater. We determined values of ΔGr for 47 sediment porewater samples along a 20cm x 2m transect for metabolic reactions involving 23 inorganic H-, O-, C-, N-, S-, Fe-, Mn-, and As- bearing compounds. 379 of the reactions considered were exergonic at one or more sampling locations. The most exergonic reactions were anaerobic CO oxidation with NO2- (136 - 162 kJ/mol e-), followed by the O2/CO, NO3-/CO, and NO2-/ H2S redox pairs. ΔGr values exhibit significant variation among sites as temperature, pH and chemical concentration vary, especially concentrations of Fe2+, Mn2+, and H2S. A great diversity of energy sources are available for microbial populations to exploit: in hotter sediments, sulfide oxidation coupled to nitrite reduction yields large amounts of energy per kg of sediment, whereas aerobic S0 oxidation is more energy-yielding in cooler areas. Our results show that at Saganaki there is a substantial amount of energy available from to microorganisms from sulfur-redox reactions. 16S rRNA pyrotag sequencing data point to diverse microbial populations at Saganaki, which is consistent with our bioenergetic profile, particularly when the thermodynamic calculations are normalized per kg of venting fluid. These data suggest a complex spatial distribution of microbial physiologies that is in good agreement with predicted energy yields.