Contaminated metals in sediments can be solubilized during an in vitro digestion by incubation with digestive fluids of marine deposit feeders. Solubilized metals are considered more bioavailable than their solid, sedimentary forms. The objectives of this study are to probe the mechanisms of the solubilization process, and examine the impact of this process on deposit feeders and metal biogeochemistry. Good correlations were observed between dissolved amino acids (AA) and metals in gut fluids of a population of healthy Arenicola marina, and 7 other species with contrasting feeding modes in their natural habitats. Coexistence of metals and AA in high-molecular-weight fractions and dramatic enrichment of soft, borderline metals in gut fluids imply the complexation of AA with metals. Normalization the metal concentrations in gut fluids and tissues of Arenicola marina with AA showed a positive relationship between the two, which suggests that AA serves as an important link shuttling metals between the two pools. The solubilization of Cu, and perhaps other metals, is an non-enzymatic, simple complexation reaction as indicated by microwave treatment on gut fluid and replacement of gut fluid with solutions of bovine serum albumin. Chemical modification of histidine residues in gut fluids dramatically blocked Cu solubilization, which indicated the importance of histidine in this process, although the involvement of non-histidine residues is also evident. After filling the strong-binding sites (e.g., histidine residues) in gut fluid of Arenicola marina, sufficient amounts of dissolved Cu can interact with the weak-binding, catalytic sites and inhibit digestive proteases. This result suggested that dissolution of sedimentary metals may have ecotoxicological effects on the population dynamics and biodiversity of deposit feeders. Most of the time-courses of metal dissolution during an in vitro digestion showed two-stage reactions: a fast reaction completed within 2min, followed by a slow, and often reduced, reaction lasting for a few hours. Thus deposit feeders with a different gut retention time may be exposed to different pools of sedimentary metals during an in vivo digestion. The kinetic patterns varied according to the combination of sedimentary metal-animal species, which is a function of the ratio of gut ligand concentration vs sedimentary metal loading. A conceptual model for the appearance of kinetic patterns is proposed according to the experimental data. The model indicates that the bioavailability of sedimentary metals is not a capacity of either sediments or species of organisms as previously thought, rather, it is a product of organism-sediment interactions.