Abstract
The biological fate of nanoparticles (NPs) taken up by organisms from their environment is a crucial issue for assessing ecological hazard. Despite its importance, it has scarcely been addressed due to the technical difficulties of doing so in whole organism in vivo studies. Here, by using transmission electron microscopy and energy dispersive X-ray spectroscopy (TEM-EDS), we describe the key aspects that characterize the interaction between an aquatic organism of global ecological and economic importance, the early larval stage of the Japanese oyster (Crassostrea gigas), and model gold NPs dispersed in their environment. The small size of the model organism allowed for a high-throughput visualization of the subcellular distribution of NPs, providing a comprehensive and robust picture of the route of uptake, mechanism of cellular permeation, and the pathways of clearance counterbalancing bioaccumulation. We show that NPs are ingested by larvae and penetrate cells through alimentary pinocytic/phagocytic mechanisms. They undergo intracellular digestion and storage inside residual bodies, before excretion with feces or translocation to phagocytic coelomocytes of the visceral cavity for potential extrusion or further translocation. Our mechanistically-supported findings highlight the potential of oyster larvae and other organisms which feature intracellular digestion processes to be exposed to man-made NPs and thus any risks associated with their inherent toxicity.
Highlights
After more than a decade of intense research into the potential environmental impact of nanotechnologies, there remain uncertainties about the extent to which biota is exposed to nanoparticles (NPs) released into water bodies
Particles sorted for full digestion are taken up by the larval digestive gland, whose function is comparable to the digestive diverticula of adult oysters, in spite of its simpler form (Millar, 1955)
While some aspects described here may can be considered peculiar to larval oysters, the larval digestive system is broadly similar to that reported for adult bivalves which feature a similar filter feeding alimentary strategy and intercellular digestion mechanism, allowing for NP cellular internalization at the digestive gland barrier (Koehler et al, 2008, Renault et al, 2008, Joubert et al, 2013)
Summary
After more than a decade of intense research into the potential environmental impact of nanotechnologies, there remain uncertainties about the extent to which biota is exposed to nanoparticles (NPs) released into water bodies. Is there a lack of evidence of the environmental concentrations of manufactured NPs, which is still dominated by modelled predictions, and of the processes by which NPs pass across biological barriers, enter cells and are subject to biological processes (Hou et al, 2013, Baalousha et al, 2016, Nowack, 2017). This last point is crucial for assessing the risks they pose, since "NP cellular internalization" is analogous to "bioaccumulation" for dissolved chemicals, i.e. the essential condition for solid particles to manifest their size- and surface- dependent reactivity against cellular components. In spite of its indisputable scientific value, there are obvious limitations in extrapolating this body of knowledge to realistic environmental scenarios where NP fate is highly influenced by the characteristics of the receiving environment (e.g. solution chemistry, composition of solid matrices) and of the organism (i.e. biological-ecological features driving the mode of interaction with nano-sized particles)
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