Microbial diversity and potential for arsenic and iron biogeochemical cycling at an arsenic rich, shallow-sea hydrothermal vent (Tutum Bay, Papua New Guinea)

The shallow submarine hydrothermal systems of Tutum Bay, Papua New Guinea, are an ideal opportunity to study the influence of arsenic on a marine ecosystem. Previous reports have demonstrated that the hydrothermal vents in Tutum Bay release arsenic in reduced hydrothermal fluids into the marine environment at the rate of 1.5 kg of arsenic/day. Aqueous arsenite is oxidized and adsorbed onto hydrous ferric oxides [HFOs] surrounding the venting area. We demonstrate here that microorganisms are key in both the oxidation of FeII and AsIII in the areas immediately surrounding the vent source. Surveys of community diversity in biofilms and in vent fluid indicate the presence of zeta-Proteobacteria, alpha-Proteobacteria, Persephonella, and close relatives of the archaeon Nitrosocaldus. The iron oxidizing zeta-Proteobacteria are among the first colonizers of solid substrates near the vents, where they appear to be involved in the precipitation of the hydrous ferric oxides (HFOs). Further, the biofilm communities possess the genetic capacity for the oxidation of arsenite. The resulting arsenate is adsorbed onto the HFOs, potentially removing the arsenic from the immediate marine system. No evidence was found for dissimilatory arsenate reduction, but the arsenate may be remobilized by detoxification mechanisms. This is the first demonstration of the genetic capacity for arsenic cycling in high temperature, shallow-sea vent communities, supporting recent culture-based findings in similar systems in Greece (Handley et al., 2010). These reports extend the deep-sea habitat of the zeta-Proteobacteria to shallow submarine hydrothermal systems, and together implicate biological oxidation of both iron and arsenite as primary biogeochemical processes in these systems, providing a mechanism for the partial removal of aqueous arsenic from the marine environment surrounding the vents.

► Microorganisms are key in the oxidation of FeII and AsIII at a shallow marine hydrothermal vent.
► zeta-Proteobacteria are primary colonizers, and precipitate hydrous ferric oxides in biofilms.
► The biofilms have the genetic capacity for arsenite oxidation and arsenate detoxification.
► We implicate biological oxidation of arsenite as a primary biogeochemical process in this system.