TY - JOUR
T1 - The developing zebrafish kidney is impaired by Deepwater Horizon crude oil early-life stage exposure
T2 - A molecular to whole-organism perspective
AU - Bonatesta, Fabrizio
AU - Emadi, Cameron
AU - Price, Edwin R.
AU - Wang, Yadong
AU - Greer, Justin B.
AU - Xu, Elvis Genbo
AU - Schlenk, Daniel
AU - Grosell, Martin
AU - Mager, Edward M.
N1 - Funding Information:
This work was supported by the Gulf of Mexico Research Initiative [Grant No. SA-1520 to the RECOVER consortium (Relationship of effects of cardiac outcomes in fish for validation of ecological risk)], the Cristina and Charles Johnson Foundation, and University of North Texas start-up funds. JG was supported in part by the U.S. Geological Survey's (USGS) Environmental Health Program (Contaminant Biology and Substances Hydrology). MG is a Maytag Professor of Ichthyology. We thank Dr. Andrea Bernardino from the University of North Texas for the assistance and consultation with the confocal microscope operation. We also thank the three anonymous reviewers for their valuable feedback and helpful suggestions for improving the manuscript. Data are publicly available through the Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC), at https://data.gulfresearchinitiative.org (doi: https://doi.org/10.7266/BFXBPAD8; and doi: https://doi.org/10.7266/P5GD67N3). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
Funding Information:
This work was supported by the Gulf of Mexico Research Initiative [Grant No. SA-1520 to the RECOVER consortium (Relationship of effects of cardiac outcomes in fish for validation of ecological risk)], the Cristina and Charles Johnson Foundation , and University of North Texas start-up funds. JG was supported in part by the U.S. Geological Survey’s (USGS) Environmental Health Program (Contaminant Biology and Substances Hydrology). MG is a Maytag Professor of Ichthyology. We thank Dr. Andrea Bernardino from the University of North Texas for the assistance and consultation with the confocal microscope operation. We also thank the three anonymous reviewers for their valuable feedback and helpful suggestions for improving the manuscript. Data are publicly available through the Gulf of Mexico Research Initiative Information and Data Cooperative (GRIIDC), at https://data.gulfresearchinitiative.org (doi: https://doi.org/10.7266/BFXBPAD8 ; and doi: https://doi.org/10.7266/P5GD67N3 ). Any use of trade, firm, or product names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
Publisher Copyright:
© 2021 Elsevier B.V.
PY - 2022/2/20
Y1 - 2022/2/20
N2 - Crude oil is known to induce developmental defects in teleost fish exposed during early life stages (ELSs). While most studies in recent years have focused on cardiac endpoints, evidence from whole-animal transcriptomic analyses and studies with individual polycyclic aromatic hydrocarbons (PAHs) indicate that the developing kidney (i.e., pronephros) is also at risk. Considering the role of the pronephros in osmoregulation, and the common observance of edema in oil-exposed ELS fish, surprisingly little is known regarding the effects of oil exposure on pronephros development and function. Using zebrafish (Danio rerio) ELSs, we assessed the transcriptional and morphological responses to two dilutions of high-energy water accommodated fractions (HEWAF) of oil from the Deepwater Horizon oil spill using a combination of qPCR and whole-mount in situ hybridization (WM-ISH) of candidate genes involved in pronephros development and function, and immunohistochemistry (WM-IHC). To assess potential functional impacts on the pronephros, three 24 h osmotic challenges (2 hypo-osmotic, 1 near iso‐osmotic) were implemented at two developmental time points (48 and 96 h post fertilization; hpf) following exposure to HEWAF. Changes in transcript expression level and location specific to different regions of the pronephros were observed by qPCR and WM-ISH. Further, pronephros morphology was altered in crude oil exposed larvae, characterized by failed glomerulus and neck segment formation, and straightening of the pronephric tubules. The osmotic challenges at 96 hpf greatly exacerbated edema in both HEWAF-exposed groups regardless of osmolarity. By contrast, larvae at 48 hpf exhibited no edema prior to the osmotic challenge, but previous HEWAF exposure elicited a concentration-response increase in edema at hypo-osmotic conditions that appeared to have been largely alleviated under near iso‐osmotic conditions. In summary, ELS HEWAF exposure impaired proper pronephros development in zebrafish, which coupled with cardiotoxic effects, most likely reduced or inhibited pronephros fluid clearance capacity and increased edema formation.
AB - Crude oil is known to induce developmental defects in teleost fish exposed during early life stages (ELSs). While most studies in recent years have focused on cardiac endpoints, evidence from whole-animal transcriptomic analyses and studies with individual polycyclic aromatic hydrocarbons (PAHs) indicate that the developing kidney (i.e., pronephros) is also at risk. Considering the role of the pronephros in osmoregulation, and the common observance of edema in oil-exposed ELS fish, surprisingly little is known regarding the effects of oil exposure on pronephros development and function. Using zebrafish (Danio rerio) ELSs, we assessed the transcriptional and morphological responses to two dilutions of high-energy water accommodated fractions (HEWAF) of oil from the Deepwater Horizon oil spill using a combination of qPCR and whole-mount in situ hybridization (WM-ISH) of candidate genes involved in pronephros development and function, and immunohistochemistry (WM-IHC). To assess potential functional impacts on the pronephros, three 24 h osmotic challenges (2 hypo-osmotic, 1 near iso‐osmotic) were implemented at two developmental time points (48 and 96 h post fertilization; hpf) following exposure to HEWAF. Changes in transcript expression level and location specific to different regions of the pronephros were observed by qPCR and WM-ISH. Further, pronephros morphology was altered in crude oil exposed larvae, characterized by failed glomerulus and neck segment formation, and straightening of the pronephric tubules. The osmotic challenges at 96 hpf greatly exacerbated edema in both HEWAF-exposed groups regardless of osmolarity. By contrast, larvae at 48 hpf exhibited no edema prior to the osmotic challenge, but previous HEWAF exposure elicited a concentration-response increase in edema at hypo-osmotic conditions that appeared to have been largely alleviated under near iso‐osmotic conditions. In summary, ELS HEWAF exposure impaired proper pronephros development in zebrafish, which coupled with cardiotoxic effects, most likely reduced or inhibited pronephros fluid clearance capacity and increased edema formation.
KW - Cardiotoxicity
KW - Crude oil
KW - Deepwater Horizon
KW - Edema
KW - Osmoregulation
KW - Pronephros
UR - http://www.scopus.com/inward/record.url?scp=85120881451&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85120881451&partnerID=8YFLogxK
U2 - 10.1016/j.scitotenv.2021.151988
DO - 10.1016/j.scitotenv.2021.151988
M3 - Article
C2 - 34838918
AN - SCOPUS:85120881451
VL - 808
JO - Science of the Total Environment
JF - Science of the Total Environment
SN - 0048-9697
M1 - 151988
ER -