Cellular and molecular aspects of metal sequestration and toxicity in earthworms

Abstract

Metals accumulated within the tissues of earthworms are not homogeneously distributed. Rather, they are sequestered predominantly within the posterior alimentary fraction. The clear organotropism of non-essential metals is reinforced by the subcellular compartmentation of metals according to their known ligand-binding affinities: in earthworm chloragocytes and intestinal epithelial cells, in situ X-ray mapping in high-pressure frozen thin cryosections revealed that Pb, Zn, Ca and P were co-distributed in a discrete subcellular compartment, whilst Cd and S were co-distributed in another. Tissue homogenization and fractionation confirmed these differences. Cd is sequestered by cysteine-rich metallothionein isoforms; one isoform may be a true Cd-detoxification protein because it bears two putative glycosylation sites, and may thus deliver Cd to the lysosomal system for cytological isolation. Metal accumulation imposes metabolic costs that can reduce somatic growth and/or reproduction in earthworms: the sequestered bioinactive metal fraction “diverts” energy into enhanced metallothionein synthesis and associated processes; the bioavailable metal fraction(s) may cause direct toxicological damage by competitive inhibition of metalloenzymes and metal-dependent transcription factors, and indirect damage if repair and compensatory stress responses are invoked. Molecular responses to metal-exposure stress are, in principle, linked to whole organism life-cycle parameters which, in turn, are ecologically relevant.