E. David Thompson

Facultative trace element hyperaccumulation in animals is reviewed, examining mechanisms of uptake and accumulation, and biological roles.

Female squirrelfish (Fam. Holocentridae) can accumulate and temporarily sequester copious amounts of zinc (Zn) in their livers. There, it is initially compartmentalized before a subsequent, estrogen-triggered redistribution to the ovaries. Here we show that cellular uptake of Zn is also influenced by estrogen signaling, and that estrogen increases concentrations of the plasma Zn-binding protein vitellogenin (VTG). However, estrogen-mediated increases in VTG are not sufficient to accommodate the magnitude of hepato-ovarian Zn transfer in female squirrelfish (Holocentrus adscensionis). These findings suggest that holocentrids have acquired the ability to use hormonal cues to drive hepatic uptake and storage of Zn, signal for its physiological redistribution, and influence the capacity for systemic transport of Zn beyond the mediation of increased plasma VTG concentrations. Such specific adaptations suggest an advantage for the oocyte, which is corroborated in further studies where we determined that oocyte Zn concentrations are positively correlated with egg viability in captive-spawned squirrelfish. The novel nature of these findings underlies the importance of Zn in squirrelfish reproductive biology.

Zinc is a vital micronutrient, yet as an environmental toxicant it can be deleterious to aquatic organisms such as fish. Consequently, the study of zinc uptake mechanisms is essential for understanding nutrition, toxicity, and metabolism of this metal. Intestinal zinc uptake was studied in two marine teleosts, using both in vitro (in vitro perfusion and intestinal sacs) and in vivo techniques (in situ bolus). Female squirrelfish (Holocentrus adscensionis) exhibited significantly increased epithelial zinc uptake associated with enhanced hepatic zinc accumulation. This confirms this zinc-hyperaccumulating teleost as a potential model of zinc absorption. Intestinal zinc uptake in the gulf toadfish (Opsanus beta) was biphasic with respect to zinc concentration (0.3-500 microM), exhibiting both saturable and passive uptake components. In both species, the passage of zinc into the postintestinal compartment was highly dependent on technique. Decreased proportions of postintestinal zinc in vivo, coupled with concentration-dependent distribution of zinc accumulation, suggested mechanisms may act to control the movement of zinc into the circulation. In addition, the results of this study were used to reinterpret previous findings of zinc uptake in freshwater fish and allowed a critique of techniques used to study intestinal metal uptake.