Subcellular Distribution of Cadmium and Nickel in Chronically Exposed Wild Fish: Inferences Regarding Metal Detoxification Strategies and Implications for Setting Water Quality Guidelines for Dissolved Metals

Abstract

The objective of this study was to investigate metal detoxification in chronically exposed juvenile yellow perch (YP: Perca flavescens) and to field test the commonly assumed threshold toxicity model. Fish were collected from lakes located along a cadmium (Cd) and nickel (Ni) concentration gradient. Ambient dissolved metal concentrations were measured to evaluate exposure and total hepatic metal concentrations were determined as a measure of metal bioaccumulation. Hepatic metal partitioning among potentially metal-sensitive fractions (heat-denatured proteins, organelles) and detoxified metal fractions (metallothionein) was determined after differential centrifugation of YP liver homogenates. Major proportions of hepatic Cd were found in the heat-stable cytosolic peptides and proteins fraction (HSP; including metallothioneins), whereas Ni was mainly found in the potentially metalsensitive heat-denaturable proteins fraction (HDP). For these chronically exposed fish there was no threshold exposure concentration below which binding of Cd or Ni to the heat-denaturable protein fraction or the organelle fraction did not occur. Metal detoxification was clearly incomplete and P. flavescens was subject to some metal-related stress, as evidenced notably by endocrine perturbations. Similar subcellular partitioning results were obtained when juvenile yellow perch were transferred from a reference lake to a Cd-contaminated lake and Cd accumulation was followed over time; there was no accumulation threshold below which Cd binding to the putative metal-sensitive fractions (HDP and organelles) did not occur. The presence of Cd and Ni in these fractions, even for low exposure concentrations and Metal Detoxification in Native Fish low hepatic accumulation, contradicts the threshold toxicity model that underpins metal toxicology theory and that is implicitly used in setting water quality guidelines for metals. Chronically exposed YP appear to have settled for a tradeoff between the cost of turning on their detoxification apparatus at full capacity, to completely suppress metal binding to metal-sensitive sites, and the alternative cost of allowing some binding of inappropriate metals to metal-sensitive sites.

Differences in metal sequestration between zebra mussels from clean and polluted field locations

“…To regulate the internal availability of essential metals for metabolic functions and to avoid inappropriate binding of essential and non-essential metals to important bio-molecules, various sub-cellular systems have evolved. With this, essential metals in excess of metabolic requirements and non-essential metals are detoxified and/or excreted (Rainbow, 2002;Campbell et al, 2005Campbell et al, , 2008. Excess of metals can be bound to the metal binding protein metallothionein (Vijver et al, 2004;Van Campenhout et al, 2008) and (subsequently) immobilized within granules (Marigómez et al, 2002).…”

Enzymatic correlates of energy status in wild yellow perch inhabiting clean and contaminated environments

“…Metals have contaminated many lakes in the area, and their effects on fish and invertebrates in the region have been regularly studied since the early 1990s [1][2][3][4]. Research has also demonstrated that the physiology of yellow perch (Perca flavescens) living in these contaminated systems is affected [5][6][7][8]. However, interpreting the causes of these physiological impairments is far from simple.…”

Multielement analysis in the fish hepatic cytosol as a screening tool in the monitoring of natural waters

“…Research on this topic most commonly refer to Cd, Cu and Zn in various fish species (e.g. in yellow perch (Kraemer et al 2006;Campbell et al 2008); rainbow trout (Kamunde and MacPhail 2008;Sappal et al 2009); zebrafish and roach (Paris-Palacios and BiagiantiRisbourg 2006)), and only sporadically to other elements such as Pb (e.g. in mummichog (Goto and Wallace 2010); brown trout and European eel (Linde et al 1999)), Ni and Tl (e.g. in yellow perch (Campbell et al 2008); fathead minnow (Lapointe and Couture 2009)) and Se (e.g.…”