Energy sources for chemolithotrophs in an arsenic- and iron-rich shallow-sea hydrothermal system

Abstract

The hydrothermally influenced sediments of Tutum Bay, Ambitle Island, Papua New Guinea, are ideal for investigating the chemolithotrophic activities of micro-organisms involved in arsenic cycling because hydrothermal vents there expel fluids with arsenite (AsIII) concentrations as high as 950 μg L−1. These hot (99 °C), slightly acidic (pH ∼6), chemically reduced, shallow-sea vent fluids mix with colder, oxidized seawater to create steep gradients in temperature, pH, and concentrations of As, N, Fe, and S redox species. Near the vents, iron oxyhydroxides precipitate with up to 6.2 wt% arsenate (AsV). Here, chemical analyses of sediment porewaters from 10 sites along a 300-m transect were combined with standard Gibbs energies to evaluate the energy yields (−ΔGr) from 19 potential chemolithotrophic metabolisms, including AsV reduction, AsIII oxidation, FeIII reduction, and FeII oxidation reactions. The 19 reactions yielded 2–94 kJ mol−1 e−, with aerobic oxidation of sulphide and arsenite the two most exergonic reactions. Although anaerobic AsV reduction and FeIII reduction were among the least exergonic reactions investigated, they are still potential net metabolisms. Gibbs energies of the arsenic redox reactions generally correlate linearly with pH, increasing with increasing pH for AsIII oxidation and decreasing with increasing pH for AsV reduction. The calculated exergonic energy yields suggest that micro-organisms could exploit diverse energy sources in Tutum Bay, and examples of micro-organisms known to use these chemolithotrophic metabolic strategies are discussed. Energy modeling of redox reactions can help target sampling sites for future microbial collection and cultivation studies.