Toxicogenomic responses of Caenorhabditis elegans to pristine and transformed zinc oxide nanoparticles

Daniel Starnes, Jason Unrine, Chun Chen, Stuart Lichtenberg, Catherine Starnes, Claus Svendsen, Peter Kille, John Morgan, Zeinah Elhaj Baddar, Amanda Spear, Paul Bertsch, Kuey Chu Chen, Olga Tsyusko

Research output: Contribution to journalArticlepeer-review

23 Scopus citations

Abstract

Manufactured nanoparticles (MNPs) undergo transformation immediately after they enter wastewater treatment streams and during their partitioning to sewage sludge, which is applied to agricultural soils in form of biosolids. We examined toxicogenomic responses of the model nematode Caenorhabditis elegans to pristine and transformed ZnO-MNPs (phosphatized pZnO- and sulfidized sZnO-MNPs). To account for the toxicity due to dissolved Zn, a ZnSO4 treatment was included. Transformation of ZnO-MNPs reduced their toxicity by nearly ten-fold, while there was almost no difference in the toxicity of pristine ZnO-MNPs and ZnSO4. This combined with the fact that far more dissolved Zn was released from ZnO- compared to pZnO- or sZnO-MNPs, suggests that dissolution of pristine ZnO-MNPs is one of the main drivers of their toxicity. Transcriptomic responses at the EC30 for reproduction resulted in a total of 1161 differentially expressed genes. Fifty percent of the genes differentially expressed in the ZnSO4 treatment, including the three metal responsive genes (mtl-1, mtl-2 and numr-1), were shared among all treatments, suggesting that responses to all forms of Zn could be partially attributed to dissolved Zn. However, the toxicity and transcriptomic responses in all MNP treatments cannot be fully explained by dissolved Zn. Two of the biological pathways identified, one essential for protein biosynthesis (Aminoacyl-tRNA biosynthesis) and another associated with detoxification (ABC transporters), were shared among pristine and one or both transformed ZnO-MNPs, but not ZnSO4. When comparing pristine and transformed ZnO-MNPs, 66% and 40% of genes were shared between ZnO-MNPs and sZnO-MNPs or pZnO-MNPs, respectively. This suggests greater similarity in transcriptomic responses between ZnO-MNPs and sZnO-MNPs, while toxicity mechanisms are more distinct for pZnO-MNPs, where 13 unique biological pathways were identified. Based on these pathways, the toxicity of pZnO-MNPs is likely to be associated with their adverse effect on digestion and metabolism. The toxicity and transcriptomics responses of transformed ZnO nanoparticles are distinct from pristine ZnO nanoparticles and only partially due to release of ions.

Original languageEnglish
Pages (from-to)917-926
Number of pages10
JournalEnvironmental Pollution
Volume247
DOIs
StatePublished - Apr 2019

Bibliographical note

Funding Information:
We acknowledge the assistance of D. Wall, D. Arndt, S. Shrestha, A. Wamucho, and Y. Thompson. Caenorhabditis elegans strains were provided by the Caenorhabditis Genetics Center, which is funded by the NIH Office of Research Infrastructure Programs ( P40 OD010440 ). Funding for this research was provided by the United States Environmental Protection Agency (EPA) Science to Achieve Results Grant RD 834574 . JU and OT are supported by the U.S. EPA and National Science Foundation (NSF) through cooperative agreement EF-0830093 , Center for Environmental Implications of Nanotechnology (CEINT). SL was partially funded by the Tracy Farmer Institute for Sustainability and the Environment . Portions of this work were performed at Beamline X26A, National Synchrotron Light Source (NSLS) , Brookhaven National Laboratory. X26A is supported by the Department of Energy (DOE) - Geosciences ( DE-FG02-92ER14244 to The University of Chicago - CARS). Use of the NSLS was supported by DOE under Contract No. DE-AC02-98CH10886 . Any opinions, findings, conclusions, or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the EPA or NSF. This work has not been subjected to EPA or NSF review, and no official endorsement should be inferred. Appendix A

Funding Information:
We acknowledge the assistance of D. Wall, D. Arndt, S. Shrestha, A. Wamucho, and Y. Thompson. Caenorhabditis elegans strains were provided by the Caenorhabditis Genetics Center, which is funded by the NIH Office of Research Infrastructure Programs (P40 OD010440). Funding for this research was provided by the United States Environmental Protection Agency (EPA) Science to Achieve Results Grant RD 834574. JU and OT are supported by the U.S. EPA and National Science Foundation (NSF) through cooperative agreement EF-0830093, Center for Environmental Implications of Nanotechnology (CEINT). SL was partially funded by the Tracy Farmer Institute for Sustainability and the Environment. Portions of this work were performed at Beamline X26A, National Synchrotron Light Source (NSLS), Brookhaven National Laboratory. X26A is supported by the Department of Energy (DOE) - Geosciences (DE-FG02-92ER14244 to The University of Chicago - CARS). Use of the NSLS was supported by DOE under Contract No. DE-AC02-98CH10886. Any opinions, findings, conclusions, or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the EPA or NSF. This work has not been subjected to EPA or NSF review, and no official endorsement should be inferred.

Publisher Copyright:
© 2019 Elsevier Ltd

Keywords

  • Gene expression
  • Nanomaterial
  • Nematode
  • Soil
  • Transcriptomics
  • Wastewater

ASJC Scopus subject areas

  • Toxicology
  • Pollution
  • Health, Toxicology and Mutagenesis

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