Nanoparticle-Biological Interactions in a Marine Benthic Foraminifer

Caterina Ciacci,Elisa Bergami,Joan M Bernhard,Yurika Ujiié,Fabrizio Frontalini,Yoshiyuki Ishitani,Rodolfo Coccioni,Margot V Grimmelpont,Pietro Gobbi,Debora Burini,Ilaria Corsi,Vincent M P Bouchet,Patrizia Ambrogini,Davide Curzi

doi:10.1038/s41598-019-56037-2

Abstract

The adverse effects of engineered nanomaterials (ENM) in marine environments have recently attracted great attention although their effects on marine benthic organisms such as foraminifera are still largely overlooked. Here we document the effects of three negatively charged ENM, different in size and composition, titanium dioxide (TiO2), polystyrene (PS) and silicon dioxide (SiO2), on a microbial eukaryote (the benthic foraminifera Ammonia parkinsoniana) using multiple approaches. This research clearly shows the presence, within the foraminiferal cytoplasm, of metallic (Ti) and organic (PS) ENM that promote physiological stress. Specifically, marked increases in the accumulation of neutral lipids and enhanced reactive oxygen species production occurred in ENM-treated specimens regardless of ENM type. This study indicates that ENM represent ecotoxicological risks for this microbial eukaryote and presents a new model for the neglected marine benthos by which to assess natural exposure scenarios.

Highlights

Among the metallic Engineered nanomaterials (ENM), titanium dioxide (TiO2) and silica dioxide (SiO2) nanoscale particles (NP) are certainly among the most abundant in terms of worldwide production with their major emission pathway to marine coastal waters via wastewater effluents[8]
NP were well dispersed in Milli-Q water, with Z-Average values below 200 nm and, close to the nominal sizes for SiO2 (92 nm vs. 109.5 nm) and PS (42 nm vs. 55.5 nm), while the formation of small agglomerates was observed for TiO2 (25 nm vs. 187.2 nm) (Fig. 1)
Nano-scale agglomerates in natural seawater (NSW) were observed for SiO2, having an average hydrodynamic diameter of 619 ± 23 nm, while micro-scale agglomerates were reached by PS (970 ± 108 nm) and TiO2 (1079 ± 108 nm)

Summary

Introduction

Among the metallic ENM, titanium dioxide (TiO2) and silica dioxide (SiO2) nanoscale particles (NP) are certainly among the most abundant in terms of worldwide production with their major emission pathway to marine coastal waters via wastewater effluents[8]. Coastal marine waters are characterized by high concentrations of ionic and organic matter (i.e., suspended colloidal particles) that interact with TiO2 and significantly affect its fate in seawater[9]. Because amorphous SiO2 has a low solubility in water, the vast majority of it is expected to settle in soil and sediment[10] Nanopolymers such as polystyrene (PS) have been included in a wide range of applications including biosensors, photonics, nanocomposites and drug delivery Eukaryotes (e.g., metazoans and protists like benthic foraminifera) have evolved the ability to internalize particles Protists, with their trophic position, short life span, general prevalence of asexual reproduction (vs mutagenic sexual reproduction), and responsiveness, are suitable models to assess the impacts of ENM. Benthic foraminiferal exposure to pollutants (e.g., trace elements, oil, and drilling muds) induces physiological stress as evidenced by a thickening of the inner organic lining, variation in the number and size of lipid droplets (LD), degeneration of mitochondria, proliferation of degradation vacuoles, reduction in the chamber formation rate, and a decrease in pseudopodial activity (see refs. 35,36 for examples)

Methods

Results

Conclusion