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TER-2: Trophic Transfer, Bioaccumulation and Biomagnification of Engineered Nanomaterials
in Basal Levels of Environmental Food Webs
John Priester, Rebecca Werlin, Randy Mielke, Patricia Holden
A fundamental concern in nanotoxicology is the possible propagation of intact nanoparticles and
their associated ecological effects through food chains. Bioaccumulation of nanoparticles
involves the concentration of nanoparticles from aqueous media into organisms. Trophic
transfer of nanoparticles involves the exchange of bioaccumulated materials from one organism
in a food web to another via predation. When the exchange during trophic transfer results in a
concentration increase, biomagnification has occurred. Bioaccumulation, trophic transfer and
biomagnification each enhance the toxicological threats of nanoparticles. The fundamental
conditions of these processes should be understood, so that nanoparticles can be designed to
avoid these outcomes. Previously, we studied the trophic transfer of CdSe quantum dots from
bacteria into their protozoan predators and published (Werlin et al., 2011, Nat. Nanotech.) that
biomagnification occurred, providing the first evidence for this pinnacle concern in ecological
outcomes of nanomaterials in the environment. Besides being an inaugural report of
biomagnification in nanoecotoxicology, the work was important because of the organisms
involved: they are ubiquitous and at the base of all food webs. Further, during the research it
became apparent how little is known regarding trophic transfer and the potential for
biomagnification that is initiated with bacterial prey. We therefore extended the work to other
nanoparticle and bacterial configurations. During this period, we built upon our initial work with
two discrete studies: 1) trophic transfer of bacterially-synthesized Se(0) nanoparticles, and 2)
protozoan uptake and bioprocessing of nano-TiO2 sorbed to its bacterial prey. Together, the
three scenarios form a complete trilogy of nanoparticle presentations into basal food webs:
bacterially-formed NPs, bacterially-biosorbed NPs, and bacterially-internalized NPs. Leveraging
our prior discovery that Pseudomonas aeruginosa PG201 intracellularly reduces selenite to
elemental selenium and thereby forms uniform intracellular Se(0) nanoparticles, we fed endpoint
bacteria to Tetrahymena. Compared to controls, we observed protozoan growth inhibition; we
also observed Se(0) accumulation in protozoan and apparent bioprocessing. Final conclusions
await full analysis of microscopy data. With nano-TiO2, we observed that protozoa do not avoid
bacteria that are circumscribed with biosorbed NPs. Rather, protozoa voraciously consume
TiO2-decorated bacteria and accumulate nano-TiO2 into food vacuoles. The accumulation of
nano-TiO2 in protozoan food vacuoles is strikingly visible in electron micrographs and exceeds
accumulations from a treatment where TiO2, but not bacterial cells, were presented in rich media.
Bacterial delivery of TiO2 in Tetrahymena appeared to increase toxicity, possibly through
alterations in prey digestion, and thus creating nutrient acquisition differences as compared to the
treatment with dissolved nutrients amended with nano-TiO2. The implication is that
biomagnification can initiate in basal food webs without bacterial intracellularization of NPs.
Overall, this project has the potential to have great impact in the following ways: 1) further
understand the conditions under which biomagnification occurs, 2) quantify biomagnification
from microbial prey into predators, 3) elaborate on the currently-sparse knowledge base
regarding biomagnification of contaminants as initiated in bacteria.