Demethylation of Methylmercury in Bird, Fish, and Earthworm.

Toxicity of methylmercury (MeHg) to wildlife and humans results from its binding to cysteine residues of proteins, forming MeHg-cysteinate (MeHgCys) complexes that hinder biological functions. MeHgCys complexes can be detoxified in vivo, yet how this occurs is unknown. We report that MeHgCys complexes are transformed into selenocysteinate [Hg(Sec)4] complexes in multiple animals from two phyla (a waterbird, freshwater fish, and earthworms) sampled in different geographical areas and contaminated by different Hg sources. In addition, high energy-resolution X-ray absorption spectroscopy (HR-XANES) and chromatography-inductively coupled plasma mass spectrometry of the waterbird liver support the binding of Hg(Sec)4 to selenoprotein P and biomineralization of Hg(Sec)4 to chemically inert nanoparticulate mercury selenide (HgSe). The results provide a foundation for understanding mercury detoxification in higher organisms and suggest that the identified MeHgCys to Hg(Sec)4 demethylation pathway is common in nature.

In Vivo Formation of HgSe Nanoparticles and Hg-Tetraselenolate Complex from Methylmercury in Seabirds-Implications for the Hg-Se Antagonism.

In vivo and in vitro evidence for detoxification of methylmercury (MeHg) as insoluble mercury selenide (HgSe) underlies the central paradigm that mercury exposure is not or little hazardous when tissue Se is in molar excess (Se:Hg > 1). However, this hypothesis overlooks the binding of Hg to selenoproteins, which lowers the amount of bioavailable Se that acts as a detoxification reservoir for MeHg, thereby underestimating the toxicity of mercury. This question was addressed by determining the chemical forms of Hg in various tissues of giant petrels Macronectes spp. using a combination of high energy-resolution X-ray absorption near edge structure and extended X-ray absorption fine structure spectroscopy, and transmission electron microscopy coupled to elemental mapping. Three main Hg species were identified, a MeHg-cysteinate complex, a four-coordinate selenocysteinate complex (Hg(Sec)4), and a HgSe precipitate, together with a minor dicysteinate complex Hg(Cys)2. The amount of HgSe decreases in the order liver > kidneys > brain = muscle, and the amount of Hg(Sec)4 in the order muscle > kidneys > brain > liver. On the basis of biochemical considerations and structural modeling, we hypothesize that Hg(Sec)4 is bound to the carboxy-terminus domain of selenoprotein P (SelP) which contains 12 Sec residues. Structural flexibility allows SelP to form multinuclear Hgx(Se,Sec)y complexes, which can be biomineralized to HgSe by protein self-assembly. Because Hg(Sec)4 has a Se:Hg molar ratio of 4:1, this species severely depletes the stock of bioavailable Se for selenoprotein synthesis and activity to one µg Se/g dry wet in the muscle of several birds. This concentration is still relatively high because selenium is naturally abundant in seawater, therefore it probably does not fall below the metabolic need for essential selenium. However, this study shows that this may not be the case for terrestrial animals, and that muscle may be the first tissue potentially injured by Hg toxicity.

Mercury in the tissues of five cephalopods species: First data on the nervous system.

Mercury (Hg), one of the elements most toxic to biota, accumulates within organisms throughout their lifespan and biomagnifies along trophic chain. Due to their key role in marine systems, cephalopods constitute a major vector of Hg in predators. Further, they grow rapidly and display complex behaviours, which can be altered by neurotoxic Hg. This study investigated Hg concentrations within 81 cephalopod specimens sampled in the Bay of Biscay, which belonged to five species: Eledone cirrhosa, Sepia officinalis, Loligo vulgaris, Todaropsis eblanae and Illex coindetii. Hg concentrations were measured in the digestive gland, the mantle muscle and the optic lobes of the brain. The digestive gland and the mantle were tissues with the most concentrated Hg among all species considered (up to 1.50 µg.g-1 dw), except E. cirrhosa. This benthic cephalopod had 1.3-fold higher Hg concentrations in the brain (up to 1.89 µg.g-1 dw) than in the mantle, while other species had 2-fold lower concentrations of Hg in the brain than in the mantle. Brain-Hg concentrations can be predicted from muscle-Hg concentrations for a given species, which facilitates the assessment of Hg toxicokinetics in cephalopods. In the most contaminated E. cirrhosa individual, the chemical form of Hg in its digestive gland, mantle muscle and optic lobes, was determined using High energy-Resolution X-ray Absorption Near Edge Structure (HR XANES) spectroscopy. In the digestive gland, 33 ± 11% of total Hg was inorganic Hg speciated as a dicysteinate complex (Hg(Cys)2), which suggested that the demethylation of dietary MeHg occurs in this organ. All Hg found in the mantle muscle and the optic lobes is methylated and bound to one cysteinyl group (MeHgCys complex), which implies that dietary MeHg is distributed to these tissues via the bloodstream. These results raised the questions regarding interspecific differences observed regarding Hg brain concentrations and the possible effect of Hg on cephalopod functional brain plasticity and behaviour.

Contaminants and energy expenditure in an Arctic seabird: Organochlorine pesticides and perfluoroalkyl substances are associated with metabolic rate in a contrasted manner.

Basal metabolic rate (BMR), the minimal energetic cost of living in endotherms, is known to be influenced by thyroid hormones (THs) which are known to stimulate in vitro oxygen consumption of tissues in birds and mammals. Several environmental contaminants may act on energy expenditure through their thyroid hormone-disrupting properties. However, the effect of contaminants on BMR is still poorly documented for wildlife. Here, we investigated the relationships between three groups of contaminants (organochlorines (OCs), perfluoroalkyl substances (PFASs), and mercury) with metabolic rate (MR), considered here as a proxy of BMR and also with circulating total THs (thyroxine (TT4) and triiodothyronine (TT3)) in Arctic breeding adult black-legged kittiwakes (Rissa tridactyla) from Svalbard, during the chick rearing period. Our results indicate a negative relationship between the sum of all detected chlordanes (∑CHLs) and MR in both sexes whereas perfluorotridecanoate (PFTrA) and MR were positively related in females only. MR was not associated with mercury. Additionally, levels of TT3 were negatively related to ∑CHLs but not to PFTrA. The findings from the present study indicate that some OCs (in both sexes) and some PFASs (only in females) could disrupt fine adjustment of BMR during reproduction in adult kittiwakes. Importantly, highly lipophilic OCs and highly proteinophilic PFASs appear, at least in females, to have the ability to disrupt the metabolic rate in an opposite way. Therefore, our study highlights the need for ecotoxicological studies to include a large variety of contaminants which can act in an antagonistic manner.

Integrative biomarker assessment of the effects of chemically and mechanically dispersed crude oil in Pacific oysters, Crassostrea gigas.

The impact of dispersed crude oil and dispersant on adult Pacific oysters, Crassostrea gigas, was evaluated through an integrative biomarker approach including (1) biochemical (plasma catecholase- and laccase-type phenoloxidase and superoxide dismutase), (2) histological (digestive cell lysosomal responses, digestive gland histopathology) and (3) physiological (flesh condition index) endpoints in the haemolymph and digestive gland. Adult oysters were exposed to non-contaminated water (control), chemically-dispersed oil (Brut Arabian Light), mechanically-dispersed oil and dispersant (FINASOL®) alone for 2days, and further depurated in non-contaminated water for 4weeks. After exposure to chemically and mechanically dispersed oil oysters exhibited induction of plasma laccase-type phenoloxidase and superoxide dismutase activities, enlargement of digestive cell lysosomes, lipofuscin accumulation, reduced neutral lipid content and atrophy of digestive gland diverticula; more markedly on exposure to chemically dispersed oil. From the studied biomarkers, only lysosomal biomarkers were significantly affected after exposure to the dispersant alone. This included lysosomal enlargement, neutral lipid depletion and lipofuscin accumulation in the digestive gland epithelium. A recovery of plasma enzyme activities was observed after 4weeks of depuration. The integrative biological response index indicated that chemically dispersed oil caused significantly higher stress to C. gigas than the mechanically-dispersed one or the dispersant alone; nevertheless, the response seems to be reversible after depuration.

To breed or not to breed: endocrine response to mercury contamination by an Arctic seabird.

Mercury, a ubiquitous toxic element, is known to alter expression of sex steroids and to impair reproduction across vertebrates but the mechanisms underlying these effects are not clearly identified. We examined whether contamination by mercury predicts the probability to skip reproduction in black-legged kittiwakes (Rissa tridactyla) from Svalbard. We also manipulated the endocrine system to investigate the mechanism underlying this relationship. During the pre-laying period, we injected exogenous GnRH (gonadotropin-releasing hormone) to test the ability of the pituitary to release luteinizing hormone (LH, a key hormone for the release of sex steroids and hence breeding) in relation to mercury burden. Birds that skipped reproduction had significantly higher mercury concentration in blood than breeders. Endocrine profiles of these birds also varied based on breeding status (breeders versus non-breeders), mercury contamination and sex. Specifically, in skippers (birds that did not breed), baseline LH decreased with increasing mercury concentration in males, whereas it increased in females. GnRH-induced LH levels increased with increasing mercury concentration in both sexes. These results suggest that mercury contamination may disrupt GnRH input to the pituitary. Thus, high mercury concentration could affect the ability of long-lived birds to modulate their reproductive effort (skipping or breeding) according to ongoing environmental changes in the Arctic, thereby impacting population dynamics.

Persistent organic pollutants and stable isotopes in pinnipeds from King George Island, Antarctica.

In the present work, fat, skin, liver and muscle samples from Leptonychotes weddellii (Weddell seal, n=2 individuals), Lobodon carcinophagus (crabeater seal, n=2), Arctocephalus gazella (Antarctic fur seal, n=3) and Mirounga leonina (southern elephant seal, n=1) were collected from King George Island, Antarctica, and analysed for POPs (PCBs, organochlorine pesticides and PBDEs) and stable isotopes (δ¹³C and δ¹5N in all tissues but fat). PBDEs could be found in only one sample (L. weddellii fat). Generally, PCBs (from 74 to 523 ng g⁻¹ lw), DDTs (from 14 to 168 ng g⁻¹ lw) and chlordanes (from 9 to 78 ng g⁻¹ lw) were the prevailing compounds. Results showed a clear stratification in accordance with ecological data. Nonetheless, stable isotope analyses provide a deeper insight into fluctuations due to migrations and nutritional stress. Correlation between δ(15)N and pollutants suggests, to some degree, a considerable ability to metabolize and/or excrete the majority of them.