Importance of metal-binding proteins in the partitioning of Cd and Zn as trophically available metal (TAM) in the brine shrimp Artemia franciscana

Abstract

Studies have shown that the trophic transfer of certain metals in aquatic systems may be controlled by the internal distribution of metal within prey and that this distribution may be influenced by detoxification mechanisms (i.e. metals bound to metal-binding proteins [metallothioneins, MT] may be more available to predators than metals associated with insoluble cellular constituents). The purpose of this investigation was to examine the interactive effects of Cd and Zn exposure on the accumulation and subcellular distribution of these metals in the brine shrimp Artemia franciscana. Particular attention was given to the partitioning of metals to a subcellular compartment containing heat-stable proteins (HSP) (e.g. MT), heat-denatured proteins (HDP) (e.g. 'enzymes') and organelles, here considered as trophically available metal (TAM). Adult A. franciscana were exposed for 3 d to Cd (control, 1, 89 or 445 µM and Zn-control) or Zn (control, 1, 89 or 445 µM and Cd-control) through solution using radioisotopes ( 109 Cd and 65 Zn) as tracers of stable metals. Following exposure, various operationally defined subcellular fractions were obtained. Increased binding of Cd to HSP resulted in increased partitioning of Cd to the TAM compartment (i.e. TAM-Cd% increased from 57 to 80% over the range of Cd exposures). This increase in TAM was greater than proportional at the 1 µM Cd exposure concentration and could result in a 'bioenhancement' of Cd trophic transfer to predators. Exposure to elevated concentrations of Cd (89 and 445 µM) also resulted in a ~50% suppression in Zn accumulation by A. franciscana. Upon increasing Zn exposure, a shift in the subcellular partitioning of Zn among TAM fractions (from HSP to HDP and organelles) maintained a TAM-Zn% of ~65%. As a verification of the TAM concept, a direct relationship was observed between the partitioning of Cd and Zn to the TAM compartment of A. franciscana exposed to the Cd-control/Zn-control treatment and absorption of these metals by the grass shrimp Palaemonetes pugio.

Significance of subcellular metal distribution in prey in influencing the trophic transfer of metals in a marine fish

“…The feeding experiment with the pure subcellular fraction demonstrated that metals distributed in the cytosolic protein fractions (HDP and HSP) could not be assimilated completely by the fish. Recently, Seebaugh et al (2005) reported that a TAM-Cd of 68-69% in prey grass shrimp P. pugio was associated with only 3-19% of AEs of Cd in the predator fish Fundulus heteroclitus, also indicating that TAM may not be totally bioavailable to fish. The AEs of metals in the fish fed the IF were also similar and were much lower than those associated with HSP and HDP, indicating a lower bioavailability when associated with the IF.…”

“…Recently, Wallace and Luoma (2003) introduced the concept of trophically available metal (TAM) (combination of organelles, HDP, and HSP) and indicated that about 100% of the TAM could be assimilated by predators. In their study, 1 : 1 relationship was established between the AE of Cd in the predator grass shrimp P. pugio and the Cd-TAM of invertebrate prey, including the oligochaete Limnodrilus hoffmeisteri, the bivalve Potemocorbula amurensis, and the brine shrimp A. franciscana (Wallace et al 1998;Wallace and Luoma 2003;Seebaugh and Wallace 2004).…”

“…and Fisher 1994; Wallace and Luoma 2003;Seebaugh and Wallace 2004). Reinfelder and Fisher (1994) quantified the assimilation of C, Cd, Co, P, S, Se, and Zn in two marine fish, Menidia menidia and M. beryllina, fed the copepod Acartia spp.…”

“…Furthermore, metals distributed in organelles, HDP, and HSP were considered to be trophically available (Wallace et al 2003). A recent study used this subcellular partitioning method to determine the transfer of Cd from grass shrimps to mummichog fish, but the relationship between the metal speciation in the shrimps and the AE in the fish was not explored (Seebaugh et al 2005).…”

Zinc and Cadmium Toxicity Using a Biotest with Artemia franciscana

“…Zinc is one of the elements that can decrease the toxicity of orally administered cadmium and its effect can be observed in competition with cadmium in certain transportation systems as well as at binding sites on metallothionein (McDowell 1992;Barata et al 2002;Seebaugh and Wallace 2004).…”