Aluminum-dependent regulation of intracellular silicon in the aquatic invertebrate Lymnaea stagnalis

Abstract

Silicon is essential for some plants, diatoms, and sponges but, in higher animals, its endogenous regulation has not been demonstrated. Silicate ions may be natural ligands for aluminum and here we show that, in the freshwater snail (Lymnaea stagnalis), intracellular silicon seems specifically up-regulated in response to sublethal aluminum exposure. X-ray microanalysis showed that exposure of snails to low levels of aluminum led to its accumulation in lysosomal granules, accompanied by marked up-regulation of silicon. Increased lysosomal levels of silicon were a specific response to aluminum because cadmium and zinc had no such effect. Furthermore, intra-lysosomal sulfur from metallothionein and other sulfur-containing ligands was increased after exposure to cadmium and zinc but not aluminum. To ensure that these findings indicated a specific in vivo response, and not ex vivo formation of hydroxy-aluminosilicates (HAS) from added aluminum (555 g͞ liter) and water-borne silicon (43 g͞liter), two further studies were undertaken. In a ligand competition assay the lability of aluminum (527 g͞liter) was completely unaffected by the presence of silicon (46 g͞liter), suggesting the absence of HAS. In addition, exogenous silicon (6.5 mg͞liter), added to the water column to promote formation of HAS, caused a decrease in lysosomal aluminum accumulation, showing that uptake of HAS would not explain the loading of aluminum into lysosomal granules. These findings, and arguments on the stability, lability, and kinetics of aluminum-silicate interactions, suggest that a silicon-specific mechanism exists for the in vivo detoxification of aluminum, which provides regulatory evidence of silicon in a multicellular organism.

Crystalline Nanorods as Possible Templates for the Synthesis of Amorphous Biosilica during Spicule Formation in Demospongiae

“…36 In complex biological systems, the codeposition of Si and Al is commonly found, and it seems to be an evolutionary mechanism as a protection against aluminum toxicity 37. 38 For example, it has been demonstrated that the pond snail Lymnea stagnalis up‐regulates the internalization of Si when exposed to high concentrations of Al, thus forming a vacuolar lysosomal codeposition of Si and Al 39. In the case of Demospongiae, the spicule‐forming cells, sclerocytes, comprise special vesicles in which the primary stages of spicules proceed.…”

Essential and Toxic Effects of Elements on Microorganisms

“…Although aluminum is the third-most abundant element in the Earth's crust (after oxygen and silicon; Weast 1984), its bioavailability is very low due to insoluble hydroxide complexes. Aluminum-stress is answered by plants by excretion of aluminum-complexing compounds as malate or citrate (Kataoka et al 2002, Pineros et al 2002, Tesfaye et al 2001, Ma et al 2001b, Yang et al 2000, Ma, 2000, silicon (Desouky et al 2002), or the synthesis of efflux systems (Sasaki et al 2002). Al(III) becomes toxic under these conditions.…”

Bioavailability and toxicity of aluminium in a model planktonic food chain (Chlamydomonas–Daphnia) at neutral pH

“…Insoluble forms of Al are generally considered to be unavailable and therefore less toxic to organisms than the dissolved ion (Al 3 + ) (Driscoll and Schecher, 1989). However, laboratory studies have demonstrated that under near-neutral pH conditions Al can be accumulated in significant amounts by some organisms, in particular filter-feeders (such as bivalves) and grazers (such as snails), causing severe physiological and behaviour disfunction (Elangovan et al, 1997;Kadar et al, 2001;Desouky et al, 2002). Exogenous toxicity has also been demonstrated in fish and crustacea due to precipitation of insoluble Al on the gills (Polé o et al, 1994;Alexopoulos et al, 2003).…”