Principle Investigator:  Roy Price

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Distribution, speciation and bioavailability of arsenic in a shallow-water submarine hydrothermal system, Tutum Bay, Ambitle Island, PNG

Shallow-water hydrothermal vent systems can introduce large amounts of potentially toxic elements, such as arsenic (As), into coastal marine environments. The first step in understanding and describing the potential impact of these elements throughout hydrothermally influenced coastal ecosystems is to determine the element’s distribution and speciation, which in turn influences the availability of the toxin for biological uptake. Shallow submarine hot springs near Ambitle Island, Papua New Guinea, are discharging as much as 1.5 kg per day of arsenic directly into a coral-reef ecosystem. We have investigated the bioavailability of the As throughout Tutum Bay by studying vent fluid, seawater, pore water, precipitates, and sediments. In addition to measuring As abundance, As speciation (As(III), As(V), and the methylated species DMA and MMA) was determined in various waters. The As concentration for discrete mineral phases in vent precipitates and sediments was determined by sequentially extracting arsenic from the easily extractable, carbonate, Fe-oxyhydroxide or hydrous ferric oxide (HFO), and residual fractions, each of which have a different bioavailability.

Diffuse venting seems to play a critical role on the distribution of As throughout Tutum Bay surface sediments, which have a mean As concentration of 527 ppm while excluding the vent precipitates (range = 1483 to 52 ppm). Up to 54 ppm As were extracted from the easily extractable fraction of surface sediments (mean = 19.7 ppm), using a K2HPO4/KH2PO4 buffer at pH = 7.2. Arsenic from this fraction is considered to be the most available for biological processes, and therefore the most dangerous for biota. However, sequential extraction shows that 98.6% of the As in vent precipitates, and a mean of 93.3% in surface sediments (range = 88.2% to 96.3%), is coprecipitated with the hydrous ferric oxide (HFO) fraction. Thus, the bulk of the As being discharged into Tutum Bay is scavenged by the HFO, and should remain stable unless the physicochemical conditions surrounding the oxides change. In surface seawaters of Tutum bay, we found as much as four times the average seawater concentration of As (8.4 μg/L compared to ∼2 μg/L). The abundance of As in seawater just above the sediment/water interface is near normal, although As(III) in both surface and bottom seawater throughout Tutum Bay is substantially enriched compared to average seawater.

Hydrothermal venting therefore provides bioavailable As by two major pathways throughout Tutum Bay: 1) easily-exchangeable As from hydrothermally influenced sediments to as far away as 200 m from focused venting, and 2) in surface seawaters, which may allow for biological uptake by phytoplankton and transfer up the food web.

Prokaryotic populations in arsenic-rich shallow-sea hydrothermal sediments of Ambitle Island, Papua New Guinea

Abstract: This study is the first to investigate the microbial ecology of the Tutum Bay (Papua New Guinea) shallow-sea hydrothermal system. The subsurface environment was sampled by SCUBA using push cores, which allowed collection of sediments and pore fluids. Geochemical analysis of sediments and fluids along a transect emanating from a discrete venting environment, about 10 mbsl, revealed a complex fluid flow regime and mixing of hydrothermal fluid with seawater within the sediments, providing a continuously fluctuating redox gradient. Vent fluids are highly elevated in arsenic, up to ∼1 ppm, serving as a “point source” of arsenic to this marine environment. 16S rRNA gene and FISH (fluorescence in situ hybridization) analyses revealed distinct prokaryotic communities in different sediment horizons, numerically dominated by Bacteria. 16S rRNA gene diversity at the genus level is greater among the Bacteria than the Archaea. The majority of taxa were similar to uncultured Crenarchaea, Chloroflexus, and various heterotrophic Bacteria. The archaeal community did not appear to increase significantly in number or diversity with depth in these sediments. Further, the majority of sequences identifying with thermophilic bacteria were found in the shallower section of the sediment core. No 16S rRNA genes of marine Crenarchaeota or Euryarchaeota were identified, and none of the identified Crenarchaeota have been cultured. Both sediment horizons also hosted “Korarchaeota”, which represent 2–5% of the 16S rRNA gene clone libraries. Metabolic functions, especially among the Archaea, were difficult to constrain given the distant relationships of most of the community members from cultured representatives. Identification of phenotypes and key ecological processes will depend on future culturing, identification of arsenic cycling genes, and RNA-based analyses.

A natural laboratory to study arsenic geobiocomplexity

Abstract: Research on seafloor hydrothermal activity has focused primarily on deep-sea black smoker-type locations, which are found along volcanically active portions of the mid-ocean ridges and in deep back-arc basins. Submarine hydrothermal activity, however, is not confined to deepwater environments. Hydrothermal vents have been documented on the tops of seamounts, on the flanks of volcanic islands, and in other near-shore environments characterized by high heat flow. Their easy accessibility, relative to deep-sea hydrothermal systems, makes them excellent natural laboratories to study a wide range of chemical, physical, and biological processes.

Enhanced geochemical gradients in a marine shallow-water hydrothermal system: Unusual arsenic speciation in horizontal and vertical pore water profiles

The shallow marine hydrothermal vents near Ambitle Island in eastern Papua New Guinea discharge hot, slightly acidic, As-rich, chemically reduced fluid into cool, slightly alkaline, oxygenated seawater. Gradients in temperature, pH, and total As (AsT), among others, are established as the two aqueous phases mix. The hydrothermal fluid contained ∼900 μg/L AsT, almost exclusively present as the reduced AsIII, while local seawater measured between 1.2 and 2.4 μg/L As, with approximately equal levels of AsIII and AsV. Of particular interest in this study was As speciation and abundance in pore waters as a function of sediment depth and as a function of distance from the area of focused venting. With increasing distance, AsTconcentration in the pore water decreased rapidly, but remained elevated up to 300 m from the area of focused venting when compared to a non-hydrothermal control site. As a function of depth (to ∼100 cm) AsT concentration in the pore water profiles was elevated and generally increased with depth. Surprisingly, aqueous AsV far exceeded aqueous AsIII at almost all distances and depths investigated, while at the control site the AsIII concentration exceeded that of AsV. In the Tutum Bay hydrothermal system, chemical disequilibria among As species provide potential metabolic energy for arsenite oxidizing microorganisms where hydrothermal fluid mixes with seawater near the vent orifice, and for arsenate reducing microorganisms with increasing distance and depth from the hydrothermal point source.

Changes in Benthic Macrofauna Associated with a Shallow-Water Hydrothermal Vent Gradient in Papua New Guinea

Abstract: Infaunal macroinvertebrates were characterized along an environmental gradient from a shallow-water hydrothermal vent located at Tutum Bay, Ambitle Island, Papua New Guinea. Samples were collected at three sites located at 7.5, 60, and 150 m from the vent and from a nonhydrothermal reference site located to the north. Temperature and arsenic concentration were found to decrease and pH increased with distance away from the vent. At each site, five replicate core samples were taken randomly from a 1 m2 sampling grid. All infaunal invertebrates > 500 µm were sorted, identified to the lowest practical taxonomic level and counted. Results from the macrofauna data show a strong trend of increasing abundance, species richness and diversity relative to distance away from the vent, but even at 150 m the benthic macrofauna appeared to be depressed relative to the reference site. Mollusks were completely absent 7.5 m from the vent, rare at 60 m, and abundant at 150 m, suggesting that the low pH values associated with the hydrothermal activity play an important role in the benthic community structure.

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 AsVreduction 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.

Enhanced bioaccumulation and biotransformation of As in coral reef organisms surrounding a marine shallow-water hydrothermal vent system

Abstract: The marine shallow-water hydrothermal system in Tutum Bay, Ambitle Island, Papua New Guinea discharges as much as 1.5 kg of arsenic (As) per day into a coral reef ecosystem. Despite the amount of As released, coral reef organisms do not seem to be affected. We investigated the uptake and bioaccumulation of geothermally-derived inorganic As by the soft coral Clavularia sp., the calcareous algaeHalimeda sp., and the sea squirt Polycarpa sp., by measuring the total As concentration (TAs) in tissues from each organism and comparing it to the same type of organism collected from a nearby control site. All organisms collected from the hydrothermal area displayed distinctly higher (2 to 20 times) TAs compared to the control site. Concentrations were typically higher in samples collected closer to the focused hydrothermal venting, which is the first direct evidence for enhanced bioaccumulation of As in organisms living within an area of hydrothermal influence. To assess As biotransformation to organoarsenicals, anionic and cationic As species were determined by IC-ICP-MS in methanol/water tissue extracts. The concentrations of several of the organoarsenic species were much higher at the hydrothermal vent site compared to the control site, and several organoarsenic species were present only in the hydrothermal samples, including some unidentifiable species. While intriguing, these speciation results cannot be interpreted robustly due to poor extraction efficiencies. Future researchers should attempt to improve the extraction efficiency to closer to 100%, which would allow a more accurate description of As biosynthesis pathways for the marine organisms living in these environments.

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