Arsenic bioaccumulation and biotransformation in deep-sea hydrothermal vent organisms from the PACMANUS hydrothermal field, Manus Basin, PNG

•The deep-sea vent gastropods A. hessleri and I. nautilie and the mussel B. manusensis contained up to 6344, 248, and 30 mg kg−1 As, respectively.•Inogranic As and arsenobetain (As-Bet) were the dominant species, with trace SO4-sug only found in A. hessleri. Trace TMAP, AC, and Tetra were found in the other organisms.•Several hypotheses are proposed for biosynthesis of As-sug and As-Bet in deep-sea vent organisms.•Future research on As bioaccumulation in deep-sea vent biota must consider improved method for total extraction.

Hydrothermal vents are often enriched in arsenic, and organisms living in these environments may accumulate high concentrations of this and other trace elements. However, very little research to date has focused on understanding arsenic bioaccumulation and biotransformation in marine organisms at deep-sea vent areas; none to date have focused organisms from back-arc spreading centers. We present for the first time concentration and speciation data for As in vent biota from several hydrothermal vent fields in the eastern Manus basin, a back-arc basin vent field located in the Bismark Sea, western Pacific Ocean. The gastropods Alviniconcha hessleri and Ifremeria nautilei, and the mussel Bathymodiolus manusensis were collected from diffuse venting areas where pH was slightly lower (6.2–6.8), and temperature (26.8–10.5 °C) and arsenic concentrations (169.5–44.0 nM) were higher than seawater. In the tissues of these organisms, the highest total measured As concentrations were in the gills of A. hessleri (5580 mg kg−1), with 721 mg kg−1 and 43 mg kg−1 in digestive gland and muscle, respectively. I. nautilei contained 118 mg kg−1 in the gill, 108 mg kg−1 in the digestive gland and 22 mg kg−1 in the muscle. B. manusensis contained 15.7 mg kg−1 in the digestive gland, followed by 9.8 mg kg-1 and 4.5 mg kg-1 in its gill and muscle tissue, respectively. We interpret the decreasing overall total concentrations in each organism as a function of distance from the source of hydrothermally derived As. The high concentration of arsenic in A. hessleri gills may be associated with elemental sulfur known to occur in this organism as a result of symbiotic microorganisms. Arsenic extracted from freeze-dried A. hessleri tissue was dominated by AsIII and AsV in the digestive gland (82% and 16%, respectively) and gills (97% AsIII, 2.3% AsV), with only 1.8% and 0.2% arsenobetaine (As-Bet) in the digestive gland and gills, respectively. However, the muscle contained substantial amounts of As-Bet (42% As-Bet compared to 48% AsIII and 10% AsV), suggesting As-Bet is a metabolite. Trace arsenosugar (SO4-sug) was observed in digestive gland and gills only. The other snail, I. nautilei, was also dominated by AsIII and AsV in digestive glands (82, 10%) and gills (80, 10%), with 6–9% As-Bet, but its muscle contained 62% As-Bet and 32% AsIII, with 7% trimethylarsoniopropionate (TMAP). Trace dimethylarsinic acid (DMAV) was observed in its gills, and trace TMAP and arsenocholine (AC) was observed in digestive glands. The mussel B. manusensis was dominated by As-Bet in all three tissue types. Digestive gland and gills contained ~22% AsIII, 5–10% AsV, 20–25% DMAV, along with some TMAP and tetramethylarsonium ion (TETRA). However, the muscle contained significantly more As-Bet (91.6%), with the only other species being AsIII (8.4%). Unfortunately, as is often the case in bioaccumulation and biotransformation studies, extraction efficiencies were low, limiting any rigorous interpretation of arsenic biotransformation patterns. Through process of elimination, we suggest that arsenosugars may be synthesized by H2S-oxidizing chemotrophic microbial mats, ultimately leading to the syntheses of As-Bet within vent organisms. However, because As-sugs rarely occur in deep-sea vent organisms, As-Bet, as well as TMAP, AC, and TETRA could also potentially be synthesized directly by the “Edmonds” pathway, the proposed arseno-analog to amino acid formation, without the necessity for arsenosugar formation as an intermediate. Future research should endeavor for more comprehensive extraction of organoarsenicals.