TY - JOUR
T1 - Adsorption of titanium dioxide nanoparticles onto zebrafish eggs affects colonizing microbiota
AU - Brinkmann, Bregje W.
AU - Beijk, Wouter F.
AU - Vlieg, Redmar C.
AU - van Noort, S. John T.
AU - Mejia, Jorge
AU - Colaux, Julien L.
AU - Lucas, Stéphane
AU - Lamers, Gerda
AU - Peijnenburg, Willie J.G.M.
AU - Vijver, Martina G.
N1 - Funding Information:
We thank Ilaria Zanoni for performing the nTiO 2 sedimentation measurements, Rian van den Nieuwendijk for providing technical support and equipment for the lyophilization of zebrafish eggs; Emilie Didaskalou for help with the concerning sample preparation; and RAS AG for providing the applied silver nanoparticles. John van Noort and Redmar Vlieg were supported by the Netherlands Organization for Scientific Research [ VICI 680.47.616 ]. This work was supported by the project PATROLS of European Union’s Horizon 2020 research and innovation programme [grant number 760813 ].
Publisher Copyright:
© 2021 The Authors
Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.
PY - 2021/3
Y1 - 2021/3
N2 - Teleost fish embryos are protected by two acellular membranes against particulate pollutants that are present in the water column. These membranes provide an effective barrier preventing particle uptake. In this study, we tested the hypothesis that the adsorption of antimicrobial titanium dioxide nanoparticles onto zebrafish eggs nevertheless harms the developing embryo by disturbing early microbial colonization. Zebrafish eggs were exposed during their first day of development to 2, 5 and 10 mg TiO2 L−1 (NM-105). Additionally, eggs were exposed to gold nanorods to assess the effectiveness of the eggs’ membranes in preventing particle uptake, localizing these particles by way of two-photon microscopy. This confirmed that particles accumulate onto zebrafish eggs, without any detectable amounts of particles crossing the protective membranes. By way of particle-induced X-ray emission analysis, we inferred that the titanium dioxide particles could cover 25–45 % of the zebrafish egg surface, where the concentrations of sorbed titanium correlated positively with concentrations of potassium and correlated negatively with concentrations of silicon. A combination of imaging and culture-based microbial identification techniques revealed that the adsorbed particles exerted antimicrobial effects, but resulted in an overall increase of microbial abundance, without any change in heterotrophic microbial activity, as inferred based on carbon substrate utilization. This effect persisted upon hatching, since larvae from particle-exposed eggs still comprised higher microbial abundance than larvae that hatched from control eggs. Notably, pathogenic aeromonads tolerated the antimicrobial properties of the nanoparticles. Overall, our results show that the adsorption of suspended antimicrobial nanoparticles on aquatic eggs can have cascading effects across different life stages of oviparous animals. Our study furthermore suggests that aggregation dynamics may occur that could facilitate the dispersal of pathogenic bacteria through aquatic ecosystems.
AB - Teleost fish embryos are protected by two acellular membranes against particulate pollutants that are present in the water column. These membranes provide an effective barrier preventing particle uptake. In this study, we tested the hypothesis that the adsorption of antimicrobial titanium dioxide nanoparticles onto zebrafish eggs nevertheless harms the developing embryo by disturbing early microbial colonization. Zebrafish eggs were exposed during their first day of development to 2, 5 and 10 mg TiO2 L−1 (NM-105). Additionally, eggs were exposed to gold nanorods to assess the effectiveness of the eggs’ membranes in preventing particle uptake, localizing these particles by way of two-photon microscopy. This confirmed that particles accumulate onto zebrafish eggs, without any detectable amounts of particles crossing the protective membranes. By way of particle-induced X-ray emission analysis, we inferred that the titanium dioxide particles could cover 25–45 % of the zebrafish egg surface, where the concentrations of sorbed titanium correlated positively with concentrations of potassium and correlated negatively with concentrations of silicon. A combination of imaging and culture-based microbial identification techniques revealed that the adsorbed particles exerted antimicrobial effects, but resulted in an overall increase of microbial abundance, without any change in heterotrophic microbial activity, as inferred based on carbon substrate utilization. This effect persisted upon hatching, since larvae from particle-exposed eggs still comprised higher microbial abundance than larvae that hatched from control eggs. Notably, pathogenic aeromonads tolerated the antimicrobial properties of the nanoparticles. Overall, our results show that the adsorption of suspended antimicrobial nanoparticles on aquatic eggs can have cascading effects across different life stages of oviparous animals. Our study furthermore suggests that aggregation dynamics may occur that could facilitate the dispersal of pathogenic bacteria through aquatic ecosystems.
KW - Cascading effects
KW - EcoPlate
KW - Host-microbiota interactions
KW - Particle-induced X-ray emission
KW - Two-photon multifocal microscopy
UR - http://www.scopus.com/inward/record.url?scp=85100006531&partnerID=8YFLogxK
U2 - 10.1016/j.aquatox.2021.105744
DO - 10.1016/j.aquatox.2021.105744
M3 - Article
AN - SCOPUS:85100006531
VL - 232
JO - Aquatic toxicology (Amsterdam, Netherlands)
JF - Aquatic toxicology (Amsterdam, Netherlands)
SN - 0166-445X
M1 - 105744
ER -