Mechanisms of heavy-metal sequestration and detoxification in crustaceans: a review

Abstract

This review is an update of information recently obtained about the physiological, cellular, and molecular mechanisms used by crustacean organ systems to regulate and detoxify environmental heavy metals. It uses the American lobster, Homarus americanus, and other decapod crustaceans as model organisms whose cellular detoxification processes may be widespread among both invertebrates and vertebrates alike. The focus of this review is the decapod hepatopancreas and its complement of metallothioneins, membrane metal transport proteins, and vacuolar sequestration mechanisms, although comparative remarks about potential detoxifying roles of gills, integument, and kidneys are included. Information is presented about the individual roles of hepatopancreatic mitochondria, lysosomes, and endoplasmic reticula in metal sequestration and detoxification. Current working models for the involvement of mitochondrial and endoplasmic reticulum calcium-transport proteins in metal removal from the cytoplasm and the inhibitory interactions between the metals and calcium are included. In addition, copper transport proteins and V-ATPases associated with lysosomal membranes are suggested as possible sequestration processes in these organelles. Together with several possible cytoplasmic divalent and trivalent anions such as sulfate, oxalate, or phosphate, accumulations of metals in lysosomes and their complexation into detoxifying precipitation granules may be regulated by variations in lysosomal pH brought about by bafilomycin-sensitive proton ATPases. Efflux processes for metal transport from hepatopancreatic epithelial cells to the hemolymph are described, as are the possible roles of hemocytes as metal sinks. While some of the cellular processes for isolating heavy metals from general circulation occur in the hepatopancreas and are beginning to be understood, very little is currently known about the roles of the gills, integument, and kidneys in metal regulation. Therefore, much remains to be clarified about the organs and mechanisms involved in metal homeostasis in decapod crustaceans.

Tissue Distribution and Correlation Profiles of Heavy-Metal Accumulation in the Freshwater Crayfish Astacus leptodactylus

“…Despite the necessity of this element in tissues, its concentrations were lower than detection limits in gill and abdominal muscle samples and therefore were not considered for correlation analysis. This element was present in exoskeleton and hepatopancreas despite the its absence in gill and abdominal sample, possibly because the former two tissue types are known sites of bioaccumulation and therefore more likely to display greater concentrations of Co (Ahearn et al 2004;Lacerda et al 2009). In addition, low overall tissue levels of Co can be explained by the fact that Co bioaccumulation is inhibited in the presence of other heavy metals-especially Ni, Cu, Zn, and Mn-possibly due to competitive interactions between those cations (Norwood et al 2007).…”

Gene Expression Profiling in Daphnia magna Part I: Concentration-Dependent Profiles Provide Support for the No Observed Transcriptional Effect Level

“…With fewer represented cells, there would appear to be a downregulation of transcripts that are specific to that tissue. From studies in other crustaceans (18), it appears the hepatopancreas is a major target site of metal toxicity. Thus, the downregulation of these digestive genes may indicate cellular toxicity to the hepatopancreas and digestive organ of D. magna.…”

Trophic Transfer of Trace Elements in an Isotopically Constructed Food Chain From a Semi-enclosed Marine Coastal Area (Stagnone di Marsala, Sicily, Mediterranean)

“…A number of factors may explain this result, in particular: (1) benthic invertebrates live closer than fish to sediment and macrophytes, which in the study area are a repository for a large number of contaminants; (2) a large number of invertebrates are known to contain metal-rich granules in which trace elements are sequestered in a detoxified form (Ahearn et al 2004) and bound to metallothioneins (Mason and Jenkins 1995); (3) trace elements in fish are also determined by a complex physiological and biochemical species-specific process (Barron 1990;Storelli and Marcotrigiano 2001); (4) trace metals in specific tissues may be much greater (e.g., liver generally concentrates metals); (5) as active swimmers, fish integrate and mirror environmental contamination at a broad spatial scale, and this may lead to misestimation of contaminant levels; and (6) organisms at greater trophic levels may exhibit more efficient excretion of certain elements (Watanabe et al 2008).…”