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The Fate of Engineered Nanomaterials in Sediments and Their Route to Bioaccumulation

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The Fate of Engineered Nanomaterials in Sediments and Their Route to Bioaccumulation The fate of engineered nanomaterials in sediments and their route to bioaccumulation Richard Kynaston Cross University of Exeter Submitted by Richard Kynaston Cross, to the University of Exeter as a thesis for the degree of Doctor of Philosophy in Biological Sciences, September 2017 This thesis is available for Library use on the understanding that it is copyright material and that no quotation from the thesis may be published without proper acknowledgement. I certify that all material in this thesis which is not my own work has been identified and that no material has previously been submitted and approved for the award of a degree by this or any other University. (Signature) ……………………………………… 1 2 Abstract The production of engineered nanomaterials is an emerging and rapidly expanding industry. It exploits the capacity for materials to be manufactured to present particular properties distinct from the bulk material, through tailoring of the particle size and surface functionality. This ability to fine tune particle properties at the nanoscale is responsible for the explosion in uses of engineered nanomaterials in industries as diverse as cosmetics and medicine, to “green” technologies and manufacturing. However, this increased reactivity at the nanoscale, defined as having at least one dimension<100 nm in size, is also responsible for the increasing concern over their environmental safety. Material flows of engineered nanoparticles into the aquatic environmenthave been identified throughout their production, use and disposal, putting these ecosystems at potential risk of contamination. In particular, sediments are a likely sink of engineered nanomaterials in the aquatic environment due to their propensity to destabilise and settle out of suspension in natural freshwaters. An emerging body of literature has demonstrated toxicity of nanomaterials to aquatic species. In this thesis, the case is presented for using bioaccumulation as a first indicator of risk to aquatic organisms exposed toengineered nanomaterials. Using the sediment dwelling freshwater worm, Lumbriculus variegatus, this work investigates the factors which govern the bioaccumulation of cerium oxide and silver nanomaterials. It is hypothesised that the fate of these materials in sediments will be determined by their core composition, primary particle size and surface coating. A novel approach is presented to measure two biologically relevant fate parameters (persistence of particles and dissolved species in the sediment pore waters) and how particle properties affect the distribution of the nanomaterials between these phases of the sediment. This provides the context within which to interpret biological exposures assessing both the extent of uptake and how they are accumulated, whether through dietary uptake or across the skin. Understanding this route to uptake is important as the mechanism of toxicity may depend upon the point of contact of a material at the nano-bio interface. For example, a nanoparticle which comes into contact with biological material in the gut may exert a different effect upon an organism than one which is translocated directly across the skin. 3 It isdemonstrated that sediment properties determine the fate of engineered nano cerium oxide and silver to a greater extent than stabilising surfactants, with the majority of particles aggregating or associating with the solid constituents of the sediment >200 nm in size. The dissolved fraction of the metal present in the pore waters was a better predictor of bioavailability than the persistence of particulate material <200 nm in size, with partially soluble nanosilver being more available than insoluble cerium oxide. The route to metal nanoparticle uptake also differed with particle core, with electrostatically stabilised citrate and sterically stabilised polyethylene glycol (PEG) coated ceria available only through dietary uptake, whilst citrate and PEG coated silver was accumulated through transdermal uptake. Dynamic changes in the fate of silver nanoparticles were also observed for sterically stabilised polyvinylpyrrolidone (PVP) coated silver, resulting in the emergence of a colloidal pore water fraction of silver after 3 months aging in sediments. However, this colloidal silver was still not considered accumulated, indicating that low molecular weight species of silver, dissolving from the particle surface either during the exposure or upon contact with the worms’ surfaces was responsible for uptake of silver from the sediments. In conclusion, this work contributes towards our understanding of the factors which determine both the route and extent of biological uptake of engineered nanomaterials. It presents a novel combination of methods which allow for understanding bioaccumulation of these materials in the context of their fate and behaviour within sediments. 4 Contents Abstract .............................................................................................................. 3 List of Tables .................................................................................................... 10 List of Figures ................................................................................................... 11 Author’s declaration .......................................................................................... 14 Acknowledgements .......................................................................................... 15 Glossary of terms ............................................................................................ 16 Introduction .................................................................................................... 19 Chapter 1:General methods and characterisation of the nanoparticle fate and behaviour in sediment ............................................................................ 31 Abstract ......................................................................................................... 31 1.1. Introduction ............................................................................................ 32 1.1.2 Rationale for nanoparticle characterisation in media representative of sediment pore waters................................................................................. 33 1.1.3 Defining biologically relevant fate parameters for nanoparticles in sediments .................................................................................................. 34 1.2. Methods and materials: .......................................................................... 35 1.2.1 Nanomaterials and reagents ............................................................. 35 1.2.2 Preparation of nanoparticle stocks and dispersions .......................... 37 1.2.3 Characterisation of nanomaterials in test media ............................... 37 1.3. Method development and optimisation: .................................................. 39 1.3.1 Assessing the stability of nanoparticles in model sediment pore waters using dynamic light scattering .................................................................... 39 1.2.4 Ultraviolet-visible light spectrometry to assess nanoparticle stability 41 1.2.5 Optimisation and validation of quantitative size analysis using transmission electron microscopy .............................................................. 41 1.2.6 Verifying the persistence of nanoparticles <100 nm in test media after aging using transmission electron microscopy ........................................... 43 1.2.7 Fate of nanoparticles in sediment matrices ....................................... 44 1.4. Generating feeding and non-feeding life stages of the worm Lumbriculus variegatus ..................................................................................................... 48 Chapter 2: Using sediment dwelling worms to establish the relative importance of dietary versus transdermal routes to nanoparticle uptake 51 Abstract ......................................................................................................... 51 2.1 Introduction ............................................................................................. 53 5 2.2 Methods .................................................................................................. 56 2.2.1 Materials and characterisation of pristine particles ........................... 56 2.2.2 Fate of CeO2 NPs in sediment during the biological exposures ........ 57 2.2.3 Generating two phenotypes for investigating the route and extent of nanoparticle uptake from sediments into Lumbriculus variegatus .............. 58 2.2.4 The relative importance of transdermal and dietary uptake of cerium III for dissolved Ce and nanoparticulate CeO2 ............................................. 58 2.2.5 The role of particle size and surface coating on the route and extent of uptake of CeO2 nanoparticles from sediments ........................................... 59 2.2.6 Data handling and statistical analysis ............................................... 60 2.3. Results ................................................................................................... 62 2.3.1 Fate and characterisation of CeO2 in sediments ............................... 62 2.3.2 Stability and agglomeration of CeO2 nanoparticles over time ........... 63 2.3.3 Producing two distinct phenotypes: feeding and non-feeding organisms .................................................................................................. 65 2.3.4 Route of uptake of dissolved cerium
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