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Biomagnification of cadmium selenide quantum dots in a simple experimental microbial food chain

Abstract

Previous studies have shown that engineered nanomaterials can be transferred from prey to predator, but the ecological impacts of this are mostly unknown. In particular, it is not known if these materials can be biomagnified—a process in which higher concentrations of materials accumulate in organisms higher up in the food chain. Here, we show that bare CdSe quantum dots that have accumulated in Pseudomonas aeruginosa bacteria can be transferred to and biomagnified in the Tetrahymena thermophila protozoa that prey on the bacteria. Cadmium concentrations in the protozoa predator were approximately five times higher than their bacterial prey. Quantum-dot-treated bacteria were differentially toxic to the protozoa, in that they inhibited their own digestion in the protozoan food vacuoles. Because the protozoa did not lyse, largely intact quantum dots remain available to higher trophic levels. The observed biomagnification from bacterial prey is significant because bacteria are at the base of environmental food webs. Our findings illustrate the potential for biomagnification as an ecological impact of nanomaterials.

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Figure 1: Extent and rate of growth of Tetrahymena varies with Pseudomonas prey treatment.
Figure 2: Tetrahymena cells after 24 h culture with Pseudomonas.
Figure 3: Stunted digestion in Tetrahymena cells preying on CdSe QD-grown, but not cadmium-acetate-grown, Pseudomonas bacteria.
Figure 4: CD:Se ratios obtained using EDS.
Figure 5: High-resolution STEM image and EDS of Tetrahymena that has fed on QD-grown Pseudomonas, after 24 h.
Figure 6: Mass- and volume-based cadmium concentrations show biomagnification in the predator relative to the prey.

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Acknowledgements

This research was primarily funded by US Environmental Protection Agency Science To Achieve Results (STAR) award no. R833323 (to P.A.H. and G.D.S.), and by the National Science Foundation and the Environmental Protection Agency under cooperative agreement no. DBI-0830117 (to P.A.H., G.N.C. and G.D.S.). Any opinions, findings and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of either the National Science Foundation or the Environmental Protection Agency. This work has not been subjected to Environmental Protection Agency review and no official endorsement should be inferred. Environmental scanning and scanning transmission electron microscopy were partly performed in the Micro-Environmental Imaging and Analysis Facility at University of California Santa Barbara (www.bren.ucsb.edu/facilities/MEIAF/) under National Science Foundation awards nos BES-9977772 and DBI-0216480. Transmission electron microscopy was partly performed in the University of California Santa Barbara Materials Research Laboratory Central Facilities supported by the Materials Research Science and Engineering Centers Program of the National Science Foundation under award no. DMR05-20415. The T. thermophila portion of the work was partially supported by grant no. R01-RR009231 from the National Center for Research Resources of the National Institutes of Health (to E.O.). The authors gratefully acknowledge critical comments on the manuscript by T. Klanjscek. Thanks also go to anonymous reviewers for valuable suggestions that led to significant improvement of the manuscript.

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P.A.H., J.H.P., R.W., E.O. and G.D.S. designed the experiment. P.K.S. and G.D.S. synthesized and provided the quantum dots. R.W. and J.H.P. executed the trophic transfer experiments. R.E.M. and S.K. performed the electron microscopy and EDS analyses. G.N.C. and S.J. determined protein carbonyl content. All authors contributed to the writing of the manuscript.

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Correspondence to P. A. Holden.

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Werlin, R., Priester, J., Mielke, R. et al. Biomagnification of cadmium selenide quantum dots in a simple experimental microbial food chain. Nature Nanotech 6, 65–71 (2011). https://doi.org/10.1038/nnano.2010.251

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