From Antarctica to California: how water birds detoxify mercury

Mercury (Hg) is a global pollutant originating from natural sources such as volcanic eruptions and forest fires, as well as from human activities like coal combustion, gold mining, and the incineration of industrial waste. Mercury bioaccumulates and biomagnifies in aquatic and terrestrial food webs in the neurotoxic and reprotoxic form of methylmercury (MeHg). Understanding the internal detoxification processes of MeHg in animals is essential for protecting wildlife and designing treatments against mercury poisoning.

In the Kerguelen Islands in Antarctica, albatrosses and petrels, being top predators of aquatic food webs, are exposed to elevated dietary sources of MeHg. One of these seabirds is the giant petrel, an aggressive scavenger known as the vulture of Antarctica. It feeds on other birds such as penguins, and it is capable of opening intact seal and whale carcasses on land and at sea. With such a diet, it is not surprising that the giant petrel is one of the birds with the highest concentration of mercury in the body.

How can these birds live with such extraordinarily high levels of mercury without dying? “The answer is in the interactions between selenium and mercury in the bodies of these predators”, explains Alain Manceau, leader of the two studies and a director of research at the CNRS. Reduced selenium, such as selenide, has long been proposed to play an antagonistic role in controlling mercury toxicity but the biochemical mechanism remained elusive. Notably, selenium is an essential micronutrient that is concentrated in marine fish due to the high concentrations of selenium in seawater. It turns out that petrels and other water birds detoxify MeHg through a sequence of reactions involving reduced selenium in the form of a prominent selenoprotein (Selenoprotein P).

The experiments with water birds started when Brett Poulin, a professor at the University of California, Davis, came to the ESRF’s ID26 beamline to study how selenium manages to detoxify mercury in the Clark’s grebe, a water bird found in lakes and wetlands of coastal California. It continued with the analysis of samples from Paco Bustamante, a professor at the University of La Rochelle, and Yves Cherel, a director of research at the CNRS from Chizé, who provided tissues of several giant petrels from the Kerguelen Islands. “We wanted to compare how the various water birds processed mercury”, explains Manceau, “especially since freshwater has less selenium than seawater”.

At the ESRF, using X-ray Absorption Spectroscopy, the scientists identified a missing intermediate reaction species (Hg(Sec)₄) of the sequential demethylation reaction MeHgCys → Hg(Sec)₄  → Hg_x(Se,Sec)_y  → HgSe (Cys = cysteine; Sec = selenocysteine). “We first discovered the Hg(Sec)₄ species in the Clark’s grebe from California. It was sheer luck because this species was 86% pure in the liver of this bird. This was our first paper. Then we found it in the liver, kidneys, muscle, and brain of the giant petrel, albeit always mixed with HgSe”, explains Manceau. “This interpretation of the data would not have been possible without all the background knowledge we gained on the biochemistry of mercury during the seven years we’ve been doing measurements on ID26”, he adds. “We combined high spectral resolution with a low detection limit and designed a very stable and reproducible set-up”, says Pieter Glatzel, the scientist in charge of beamline ID26.

Since mercury is ultimately detoxified as HgSe, it is generally considered that mercury is without toxicological consequences as long as there is sufficient selenium, because HgSe is chemically inert. The data from the ESRF allowed the scientists to quantify the bioavailable selenium in several tissues of the birds from the concentrations of each Se-bound mercury species. The researchers noticed that Hg(Sec)₄ severely depletes the amount of bioavailable selenium in the birds, more so than previously thought when only considering mercury speciated as HgSe. Selenium deficiency can cause neurotoxicological effects and infertility, as selenoproteins serve critical anti-oxidant functions in the brain and testis. More research is ultimately needed to probe the biochemical response of selenium deficiency as a result of mercury detoxification in animals.

“The results of these studies shed light on how fauna manages to naturally get rid of the toxicity of mercury”, says Manceau. “Selenoprotein P is a key protein: it forms the Hg(Sec)₄ complex and directs the biomineralization of toxic mercury into nontoxic HgSe”, he concludes. For now, Manceau will continue his research by investigating how other animals, such as crocodiles, marine turtles, and snakes, which are all naturally poisoned by mercury, transform and internally traffic mercury.

References:

Manceau A., et al, Environmental Science & Technology Article ASAP. DOI: 10.1021/acs.est.0c04948

Manceau A., et al, Environmental Science & Technology, Article ASAP. DOI: 10.1021/acs.est.0c06269

Text and video by Montserrat Capellas Espuny