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

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,more » 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.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [3];  [2];  [4];  [5]; ORCiD logo [6];  [6];  [2];  [2];  [7];  [2];  [2]
  1. Univ. of Kentucky, Lexington, KY (United States); Belmont University, Nashville, TN (United States)
  2. Univ. of Kentucky, Lexington, KY (United States)
  3. Univ. of Kentucky, Lexington, KY (United States); Northwest A&F University Shaanxi (China)
  4. Belmont University, Nashville, TN (United States); Univ. of Kentucky, Lexington, KY (United States)
  5. Centre for Ecology and Hydrology (United Kingdom)
  6. Cardiff University (United Kingdom)
  7. Commonwealth Scientific and Industrial Research Organization (CSIRO), Brisbane, QLD (Australia)
Publication Date:
Research Org.:
University of Chicago, IL (United States); Brookhaven National Laboratory (BNL), Upton, NY (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1610189
Alternate Identifier(s):
OSTI ID: 1636354
Grant/Contract Number:  
FG02-92ER14244; AC02-98CH10886
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Pollution
Additional Journal Information:
Journal Volume: 247; Journal ID: ISSN 0269-7491
Publisher:
Elsevier
Country of Publication:
United States
Language:
English
Subject:
54 ENVIRONMENTAL SCIENCES; gene expression; nanomaterial; nematode; transcriptomics; soil; wastewater

Citation Formats

Starnes, Daniel, Unrine, Jason, Chen, Chun, Lichtenberg, Stuart, Starnes, Catherine, Svendsen, Claus, Kille, Peter, Morgan, John, Baddar, Zeinah Elhaj, Spear, Amanda, Bertsch, Paul, Chen, Kuey Chu, and Tsyusko, Olga. Toxicogenomic responses of Caenorhabditis elegans to pristine and transformed zinc oxide nanoparticles. United States: N. p., 2019. Web. doi:10.1016/j.envpol.2019.01.077.
Starnes, Daniel, Unrine, Jason, Chen, Chun, Lichtenberg, Stuart, Starnes, Catherine, Svendsen, Claus, Kille, Peter, Morgan, John, Baddar, Zeinah Elhaj, Spear, Amanda, Bertsch, Paul, Chen, Kuey Chu, & Tsyusko, Olga. Toxicogenomic responses of Caenorhabditis elegans to pristine and transformed zinc oxide nanoparticles. United States. https://doi.org/10.1016/j.envpol.2019.01.077
Starnes, Daniel, Unrine, Jason, Chen, Chun, Lichtenberg, Stuart, Starnes, Catherine, Svendsen, Claus, Kille, Peter, Morgan, John, Baddar, Zeinah Elhaj, Spear, Amanda, Bertsch, Paul, Chen, Kuey Chu, and Tsyusko, Olga. Tue . "Toxicogenomic responses of Caenorhabditis elegans to pristine and transformed zinc oxide nanoparticles". United States. https://doi.org/10.1016/j.envpol.2019.01.077. https://www.osti.gov/servlets/purl/1610189.
@article{osti_1610189,
title = {Toxicogenomic responses of Caenorhabditis elegans to pristine and transformed zinc oxide nanoparticles},
author = {Starnes, Daniel and Unrine, Jason and Chen, Chun and Lichtenberg, Stuart and Starnes, Catherine and Svendsen, Claus and Kille, Peter and Morgan, John and Baddar, Zeinah Elhaj and Spear, Amanda and Bertsch, Paul and Chen, Kuey Chu and Tsyusko, Olga},
abstractNote = {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.},
doi = {10.1016/j.envpol.2019.01.077},
journal = {Environmental Pollution},
number = ,
volume = 247,
place = {United States},
year = {Tue Jan 29 00:00:00 EST 2019},
month = {Tue Jan 29 00:00:00 EST 2019}
}

Journal Article:

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Cited by: 23 works
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Figures / Tables:

Table 1 Table 1: Pathways identified by Partek, DAVID and Pathview using lists of significantly differentially expressed genes after Caenorhabditis elegans were exposed for 48 hours to ZnSO4, pristine Zinc Oxide manufactured nanoparticles (ZnO-MNPs), phosphatized (pZnO-MNPs), or sulfidized (sZnO-MNPs) in synthetic soil pore water. The fold enrichment and p-values are estimated frommore » Partek. The number in parenthesis in “Genes in Pathway” column are additional genes that according to DAVID or Pathview analysis are also included in the pathways. The upregulated and down-regulated genes in pathways are shown in red and blue font, respectively.« less

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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.