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

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.

[1]  Nastassja A. Lewinski,et al.  Quantification of water solubilized CdSe/ZnS quantum dots in Daphnia magna. , 2010, Environmental science & technology.

[2]  H. Ducklow,et al.  Production and Fate of Bacteria in the Oceans , 1983 .

[3]  S. Kjelleberg,et al.  Impact of Violacein-Producing Bacteria on Survival and Feeding of Bacterivorous Nanoflagellates , 2004, Applied and Environmental Microbiology.

[4]  Christine Ogilvie Robichaud,et al.  Estimates of upper bounds and trends in nano-TiO2 production as a basis for exposure assessment. , 2009, Environmental science & technology.

[5]  D. Caron,et al.  Role of protozoan grazing in relieving iron limitation of phytoplankton , 1996, Nature.

[6]  Anindita Sengupta,et al.  Aqueous toxicity and food chain transfer of quantum dots™ in freshwater algae and Ceriodaphnia dubia , 2008, Environmental toxicology and chemistry.

[7]  H. Güde Grazing by protozoa as selection factor for activated sludge bacteria , 1979, Microbial Ecology.

[8]  K. Jürgens,et al.  Direct and Indirect Effects of Protist Predation on Population Size Structure of a Bacterial Strain with High Phenotypic Plasticity , 2006, Applied and Environmental Microbiology.

[9]  H. Hansma,et al.  Elongation Correlates with Nutrient Deprivation in Pseudomonas aeruginosa Unsaturated Biofilms , 2002, Microbial Ecology.

[10]  M A Kiser,et al.  Titanium nanomaterial removal and release from wastewater treatment plants. , 2009, Environmental science & technology.

[11]  J. Pernthaler Predation on prokaryotes in the water column and its ecological implications , 2005, Nature Reviews Microbiology.

[12]  R. Allen,et al.  The Correlation of Digestive Vacuole pH and Size with the Digestive Cycle in Paramecium caudatum1 , 1982 .

[13]  E. Orias,et al.  Heat-sensitive development of the phagocytotic organelle in a Tetrahymena mutant. , 1975, Experimental cell research.

[14]  D. Swackhamer,et al.  Effect of microbes on contaminant transfer in the Lake Superior food web. , 2005, Environmental science & technology.

[15]  J. Morrow,et al.  Trophic transfer of nanoparticles in a simplified invertebrate food web. , 2008, Nature nanotechnology.

[16]  M Boller,et al.  Synthetic TiO2 nanoparticle emission from exterior facades into the aquatic environment. , 2008, Environmental pollution.

[17]  Patricia A Holden,et al.  Effects of soluble cadmium salts versus CdSe quantum dots on the growth of planktonic Pseudomonas aeruginosa. , 2009, Environmental science & technology.

[18]  M. Croteau,et al.  Trophic transfer of metals along freshwater food webs: Evidence of cadmium biomagnification in nature , 2005 .

[19]  N. Fisher,et al.  Trophic transfer of Fe, Zn and Am from marine bacteria to a planktonic ciliate , 2009 .

[20]  J. D. Eccleston-Parry,et al.  A comparison of the growth kinetics of six marine heterotrophic nanoflagellates fed with one bacterial species. , 1994 .

[21]  Huan‐Tsung Chang,et al.  Photoassisted synthesis of CdSe and core-shell CdSe/CdS quantum dots. , 2005, Langmuir : the ACS journal of surfaces and colloids.

[22]  Franck Chauvat,et al.  Cytotoxicity of CeO2 nanoparticles for Escherichia coli. Physico-chemical insight of the cytotoxicity mechanism. , 2006, Environmental science & technology.

[23]  M. Clarholm Interactions of bacteria, protozoa and plants leading to mineralization of soil nitrogen , 1985 .

[24]  E. Madsen,et al.  In situ biodegradation: microbiological patterns in a contaminated aquifer , 1991, Science.

[25]  B. T. Johnson,et al.  Biomagnification of p, p'-DDT and methoxychlor by bacteria. , 1973, Applied microbiology.

[26]  William H. Majoros,et al.  Macronuclear Genome Sequence of the Ciliate Tetrahymena thermophila, a Model Eukaryote , 2006, PLoS biology.

[27]  Scott E McNeil,et al.  Nanotechnology safety concerns revisited. , 2008, Toxicological sciences : an official journal of the Society of Toxicology.

[28]  J. Boenigk,et al.  Confusing Selective Feeding with Differential Digestion in Bacterivorous Nanoflagellates , 2001, The Journal of eukaryotic microbiology.

[29]  W. Schlesinger Biogeochemistry: An Analysis of Global Change , 1991 .

[30]  G. K. L I M B A C H,et al.  Removal of Oxide Nanoparticles in a Model Wastewater Treatment Plant : Influence of Agglomeration and Surfactants on Clearing Efficiency , 2008 .

[31]  Jamie R Lead,et al.  Nanomaterials in the environment: Behavior, fate, bioavailability, and effects , 2008, Environmental toxicology and chemistry.

[32]  Lingtian Xie,et al.  Trophic transfer of Cd from natural periphyton to the grazing mayfly Centroptilum triangulifer in a life cycle test. , 2010, Environmental pollution.

[33]  J. Boenigk,et al.  The Influence of Preculture Conditions and Food Quality on the Ingestion and Digestion Process of Three Species of Heterotrophic Nanoflagellates , 2001, Microbial Ecology.

[34]  P. Holden,et al.  Bacterial and Mineral Elements in an Arctic Biofilm: A Correlative Study Using Fluorescence and Electron Microscopy , 2010, Microscopy and Microanalysis.

[35]  E. Sherr,et al.  Significance of predation by protists in aquatic microbial food webs , 2004, Antonie van Leeuwenhoek.

[36]  B. Finlay,et al.  Protozoan control of bacterial abundances in freshwater. , 1991 .

[37]  X. Tang,et al.  Impact of carbon nanotubes on the ingestion and digestion of bacteria by ciliated protozoa. , 2008, Nature nanotechnology.

[38]  L E Rikans,et al.  Mechanisms of cadmium‐mediated acute hepatotoxicity , 2000, Journal of biochemical and molecular toxicology.

[39]  W. Whitman,et al.  Prokaryotes: the unseen majority. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[40]  Huiguang Zhu,et al.  Quantum dot weathering results in microbial toxicity. , 2008, Environmental science & technology.

[41]  N. Bury,et al.  Metal contamination in aquatic environments: science and lateral management , 2009 .

[42]  D. Bagchi,et al.  Oxidative mechanisms in the toxicity of metal ions. , 1995, Free radical biology & medicine.

[43]  G. W. Bailey,et al.  Bacterial sorption of heavy metals , 1989, Applied and environmental microbiology.