Mercury speciation and stable isotopes in emperor penguins: First evidence for biochemical demethylation of methylmercury to mercury-dithiolate and mercury-tetraselenolate complexes

Apex marine predators, such as toothed whales and large petrels and albatrosses, ingest mercury (Hg) primarily in the form of methylmercury (MeHg) via prey consumption, which they detoxify as tiemannite (HgSe). However, it remains unclear how lower trophic level marine predators, termed mesopredators, with elevated Hg concentrations detoxify MeHg and what chemical species are formed. To address this need, we used high energy-resolution X-ray absorption near edge structure spectroscopy paired with nitrogen (N) and Hg stable isotopes to identify the chemical forms of Hg, Hg sources, and species-specific δ²⁰²Hg isotopic values in emperor penguin, a mesopredator feeding primarily on Antarctic silverfish. The penguin liver contains variable proportions of MeHg and two main inorganic Hg complexes (IHg), Hg-dithiolate (Hg(SR)₂) and Hg-tetraselenolate (Hg(Sec)₄), each characterized by specific isotopic values (δ²⁰²MeHg = 0.3 ± 0.2 ‰, δ²⁰²Hg(SR)₂ = -1.6 ± 0.2 ‰, δ²⁰²Hg(Sec)₄ = -2.0 ± 0.1 ‰). Using δ¹⁵N as a tracer of food source, we show that Hg(SR)₂ is likely not obtained through dietary intake, but rather is present as a biochemical demethylation product. Furthermore, on average, female penguins transferred Hg to the egg strictly as MeHg in the egg albumen but as mixtures of MeHg and IHg in the membrane (89 % and 11 %, respectively) and yolk (32 % MeHg and 68 % Hg(Sec)₄). Despite IHg species in eggs, MeHg is still the main species quantitatively transferred by the mother to the chick because of the disproportionate mass of the MeHg-rich albumen compared to the yolk. This work highlights the transformation of MeHg to Hg(SR)₂ during demethylation for the first time in multicellular organisms, but further work is needed to understand the formation of Hg(SR)₂ in the presence of relatively abundant Se biomolecules in lower trophic level predator species.