Mercury Isotope Fractionation by Internal Demethylation and Biomineralization Reactions in Seabirds: Implications for Environmental Mercury Science

Abstract

A prerequisite for environmental and toxicological applications of mercury (Hg) stable isotopes in wildlife and humans is quantifying the isotopic fractionation of biological reactions. Here, we measured stable Hg isotope values of relevant tissues of giant petrels (Macronectes spp.). Isotopic data were interpreted with published HR-XANES spectroscopic data that document a step-wise transformation of methylmercury (MeHg) to Hg-tetraselenolate (Hg(Sec)4) and mercury selenide (HgSe) (Sec = selenocysteine). By mathematical inversion of isotopic and spectroscopic data, identical δ 202 Hg values for MeHg (2.69 ± 0.04 ‰), Hg(Sec)4 (−1.37 ± 0.06 ‰), and HgSe (0.18 ± 0.02 ‰) were determined in 23 tissues of eight birds from the Kerguelen Islands and Adélie Land (Antarctica). Isotopic differences in δ 202 Hg between MeHg and Hg(Sec)4 (−4.1 ± 0.1 ‰) reflect mass-dependent fractionation from a kinetic isotope effect due to the MeHg → Hg(Sec)4 demethylation reaction. Surprisingly, Hg(Sec)4 and HgSe differed isotopically in δ 202 Hg (+1.6 ± 0.1 ‰) and mass-independent anomalies (i.e., changes in Δ 199 Hg of ≤0.3 ‰), consistent with equilibrium isotope effects of massdependent and nuclear volume fractionation from Hg(Sec)4 → HgSe biomineralization. The invariance of species-specific δ 202 Hg values across tissues and individual birds reflects the kinetic lability of Hgligand bonds and tissue-specific redistribution of MeHg and inorganic Hg, likely as Hg(Sec)4. These observations provide fundamental information necessary to improve the interpretation of stable Hg isotope data and provoke a revisitation of processes governing isotopic fractionation in biota and toxicological risk assessment in wildlife.

Comment on “New insights into the biomineralization of mercury selenide nanoparticles through stable isotope analysis in giant petrel tissues”

“…This interpretation conflicts with two recent Hg isotope studies performed on 22 petrel tissues from 8 individuals and 89 whale tissues from 28 individuals [4,15]. The δ 202 Hg value of a tissue (δ 202 Hgt) is the weighted sum of the MDF of each Hg species (Spi) expressed as follows:…”

“…in which f(Spi)t is the fractional amount of species i in tissue t, and δ 202 Spi is the species-specific MDF. Through a mathematical inversion analysis of the petrel and whale isotopic data, Manceau et al [4,15] showed that the 22 δ 202 Hgt petrel values and the 89 δ 202 Hgt whale values, could be calculated with just three δ 202 Spi values, each associated with the MeHgCys, Hg(Sec)4, and HgSe species. Therefore, Equation 1 was reduced to We show below that the Queipo-Abad et al [1] data can be reinterpreted in light of the findings of the recent petrel and whale studies [4,15], which concluded that the three Hg species have a specific isotopic composition which is homogenized throughout the body.…”

Internal Dynamics and Metabolism of Mercury in Biota: A Review of Insights from Mercury Stable Isotopes

“…Given that tissues often contain MeHg and one or more inorganic Hg species, product–reactant isotopic enrichment factors (ε p/r ) have been determined mathematically on tissues analyzed for both chemical speciation and stable Hg isotope data. 58 , 59 The demethylation of MeHg to Hg(Sec) 4 results in isotopically lighter Hg(Sec) 4 due to MDF from a kinetic isotope effect, with δ 202 Hg of product Hg(Sec) 4 being 2.2 to 4.1‰ depleted relative to the reactant MeHg (δ 202 Hg ε p/r = −2.2 to −4.1‰). 58 , 59 Conversely, the biomineralization of HgSe from Hg(Sec) 4 results in a positive MDF (δ 202 Hg ε p/r = +1.6 ± 0.1‰) in the HgSe product relative to Hg(Sec) 4 as observed in the kidney and liver of seabirds ( Figure 1 a).…”

“… 58 , 59 The demethylation of MeHg to Hg(Sec) 4 results in isotopically lighter Hg(Sec) 4 due to MDF from a kinetic isotope effect, with δ 202 Hg of product Hg(Sec) 4 being 2.2 to 4.1‰ depleted relative to the reactant MeHg (δ 202 Hg ε p/r = −2.2 to −4.1‰). 58 , 59 Conversely, the biomineralization of HgSe from Hg(Sec) 4 results in a positive MDF (δ 202 Hg ε p/r = +1.6 ± 0.1‰) in the HgSe product relative to Hg(Sec) 4 as observed in the kidney and liver of seabirds ( Figure 1 a). A separate study by Queipo-Abad et al that measured δ 202 Hg of HgSe isolated from bird liver tissues largely agreed with the value of δ 202 Hg of HgSe determined by a combination of X-ray and isotope analyses (∼0.2‰).…”

“… 59 Consequently, the δ 202 Hg values of bird tissues often exhibit a negative trend with decreasing %MeHg due to the demethylation reaction and a positive trend in δ 202 Hg in tissues with low %MeHg (<10%) due to HgSe biomineralization. 59 , 60 , 69 The different chemical forms of Hg exhibit unique Hg isotope signatures (δ 202 Hg MeHg > δ 202 Hg HgSe > δ 202 Hg Hg(Sec)4 ) that were observed to be relatively invariant between tissues within bird species. 58 , 59 The directly measured δ 202 Hg MeHg 76 confirms its invariance within an individual bird regardless of the degree of MeHg transformations.…”