The gut barrier and the fate of engineered nanomaterials: a view from comparative physiology

Abstract

The structure of the gut barrier and luminal chemistry in non-mammalian vertebrates and invertebrates has been given little attention with respect to the dietary uptake of engineered nanomaterials (ENMs). This review compares the diversity of gut anatomy in selected species used for regulatory toxicity testing, especially in relation to gut lumen chemistry and the behaviour of ENMs, and the gut as a barrier to ENMs. High ionic strength, the presence of divalent ions and organic matter promote particle aggregation in the lumen. The redox chemistry of the gut offers reducing conditions for ENM transformation, and corona formation will depend on the gut contents. Areas of low pH in the gut lumen in several species will promote the dissolution of metallic ENMs. There is a protective unstirred layer over the surface of the epithelium that may concentrate ENMs. Some organisms, especially vertebrates, can slough mucus to remove this adsorbed nanomaterial and lower bioavailability. Invertebrates also have protective layers of cuticle or peritrophic membranes that will modulate ENM uptake. Paracellular uptake of ENMs is unlikely. Transcellular uptake via vesicular-dependent pathways remains the most likely route across the gut epithelium. Most species have receptor-mediated endocytosis pathways and/or macropinocytosis in the gut epithelium. Crucially, many invertebrates have another potential pathway via ‘intracellular digestion’ uptake routes leading into the gut epithelium, and with gut associated immune cells being a potential route for ENM translocation across the epithelium. The basal lamina provides another barrier prior to the internal compartments of many animals. The features of the gut lumen and epithelium can limit the uptake of ENMs across the gut barrier in vivo, although some ENMs are detected in the tissues. Invertebrates also have the ability for biogenic mineral formation at the nano scale inside tissues. In conclusion, despite the diverse structural anatomies of the gut barrier of animals, some common features in the gut lumen chemistry tend to promote particle aggregation and settling onto the gut surface. The functional anatomy ensures the gut remains a formidable barrier to ENMs, and with some potential novel uptake processes in invertebrates that are not present in vertebrate animals.