Subcellular Partitioning of Trace Elements Is Related to Metal Ecotoxicological Classes in Livers of Fish (Esox lucius; Coregonus clupeaformis) from the Yellowknife Area (Northwest Territories, Canada)

Abstract

The subcellular partitioning of trace elements (TEs) may depend on their binding preferences, although few field data are available from mining-impacted areas. Northern pike and lake whitefish were collected from different aquatic systems located in the Yellowknife mining area (Northwest Territories, Canada) to examine the subcellular partitioning of TEs in liver cells. Elements belonging to metal classes based on binding affinities were considered: A (Ce, La), borderline (As, Pb), and class B (Ag, Cd). Measurements in the metal-detoxified fractions (granule-like structures and heat-stable proteins and peptides) and in the putative metal-sensitive fractions (heat-denatured proteins, mitochondria and microsomes, and lysosomes) revealed marked differences among metal classes. In both fish species, Cd and Ag accumulated more as detoxified forms (higher than 50%, likely bound to metallothionein-like proteins) than La and Ce (not more than 20%). The two borderline TEs (As and Pb) showed an intermediate behavior between classes A and B. Similar proportions were found in the "sensitive" subcellular fractions for all TEs, where quantitative ion character-activity relationships (QICARs) indicated the covalent index and electronegativity as predictors of the TE contribution in this compartment. This study supports the use of classes of metals to predict the toxicological risk of data-poor metals in mining areas.

Keywords: detoxification; fish; metal-binding properties; metal-handling strategies; quantitative ion character-activity relationships; toxicity.

Figure 2

Box and whisker distribution of the contribution (%, n = 10–28) of Ag (upper panels) and Cd (lower panels) in each subcellular fraction and compartment of the liver of lake whitefish (Coregonus clupeaformis) and northern pike (Esox lucius). Each dot represents an individual fish value. Bars with different letters indicate that the differences are significant (lowercase letters for subcellular fractions: Kruskal-Wallis test followed by Dunn’s test using Bonferroni correction; capitalized letters for compartments: Wilcoxon-Mann-Whitney test, p < 0.05). MIT: mitochondria; ML: microsomes and lysosomes; HDP: heat-denatured proteins; GRAN: granules; HSP: heat-stable proteins and peptides; MSC: metal-sensitive compartment; MDC: metal-detoxified compartment.

Figure 3

Box and whisker distribution of the contribution (%, n = 19–29) of As (upper panels) and Pb (lower panels) in each subcellular fraction and compartment of the liver of lake whitefish (Coregonus clupeaformis) and northern pike (Esox lucius). Each dot represents an individual fish value. Bars with different letters indicate that the differences are significant (lowercase letters for subcellular fractions: Kruskal-Wallis test followed by Dunn’s test using Bonferroni correction; capitalized letters for compartments: Wilcoxon-Mann-Whitney test, p < 0.05). MIT: mitochondria; ML: microsomes and lysosomes; HDP: heat-denatured proteins; GRAN: granules; HSP: heat-stable proteins and peptides; MSC: metal-sensitive compartment; MDC: metal-detoxified compartment.

Figure 4

Box and whisker distribution of the contribution (%; n = 16–26) of La (upper panels) and Ce (lower panels) in each subcellular fraction and compartment of the liver of lake whitefish (Coregonus clupeaformis) and northern pike (Esox lucius). Each dot represents an individual fish value. Bars with different letters indicate that the differences are significant (lowercase letters for subcellular fractions: Kruskal-Wallis test followed by Dunn’s test using Bonferroni correction; capitalized letters for compartments: Wilcoxon-Mann-Whitney test, p < 0.05). MIT: mitochondria; ML: microsomes and lysosomes; HDP: heat-denatured proteins; GRAN: granules; HSP: heat-stable proteins and peptides; MSC: metal-sensitive compartment; MDC: metal-detoxified compartment.

Figure 1

Box and whisker distribution of total concentrations (means ± SD, nmol g^-1 dw) of Ag, Cd, As, Pb, La, and Ce in the liver of lake whitefish (Coregonus clupeaformis; n = 6–10) and northern pike (Esox lucius; n = 5–8) collected from the Yellowknife area. Each dot represents an individual fish value. Bars with different letters indicate that the differences are significant (Kruskal-Wallis test followed by Dunn’s test using Bonferroni correction, p < 0.05).

Figure 5

Box and whisker distribution of the metal contribution (%; n = 11–29) of metals belonging to different classes (Class B, Borderline, A) in the metal-detoxified compartment and in the metal-sensitive compartment of the liver of lake whitefish (Coregonus clupeaformis) and northern pike (Esox lucius). Each dot represents individual fish value. Bars with different letters indicate that the differences are significant (Kruskal-Wallis test followed by Dunn’s test using Bonferroni correction, p < 0.05).