Toxicity of crude oil-derived polar unresolved complex mixtures to Pacific herring embryos: Insights beyond polycyclic aromatic hydrocarbons

Maxwell L Harsha; Yanila Salas-Ortiz; Alysha D Cypher; Ed Osborn; Eduardo Turcios Valle; Jacob L Gregg; Paul K Hershberger; Yuri Kurerov; Sarah King; Aleksandar I Goranov; Patrick G Hatcher; Anastasia Konefal; T Erin Cox; Justin B Greer; James P Meador; Matthew A Tarr; Patrick L Tomco; David C Podgorski

doi:10.1016/j.scitotenv.2024.177447

Toxicity of crude oil-derived polar unresolved complex mixtures to Pacific herring embryos: Insights beyond polycyclic aromatic hydrocarbons

Sci Total Environ. 2024 Nov 14:957:177447. doi: 10.1016/j.scitotenv.2024.177447. Online ahead of print.

Authors

Maxwell L Harsha¹, Yanila Salas-Ortiz¹, Alysha D Cypher², Ed Osborn¹, Eduardo Turcios Valle¹, Jacob L Gregg³, Paul K Hershberger³, Yuri Kurerov⁴, Sarah King⁵, Aleksandar I Goranov⁶, Patrick G Hatcher⁶, Anastasia Konefal⁷, T Erin Cox⁷, Justin B Greer⁸, James P Meador⁹, Matthew A Tarr¹, Patrick L Tomco¹⁰, David C Podgorski¹¹

Affiliations

¹ Department of Chemistry, Chemical Analysis & Mass Spectrometry Facility, University of New Orleans, New Orleans, Louisiana 70148, USA.
² Prince William Sound Science Center, Cordova, AK 99574, USA.
³ U.S. Geological Survey, Western Fisheries Research Center, Marrowstone Marine Field Station, Nordland, Washington 98358, USA.
⁴ Department of Chemistry, Chemical Analysis & Mass Spectrometry Facility, University of New Orleans, New Orleans, Louisiana 70148, USA; Eurofins Central Analytical Laboratories, New Orleans, Louisiana 70122, USA.
⁵ Eurofins Central Analytical Laboratories, New Orleans, Louisiana 70122, USA.
⁶ Department of Chemistry and Biochemistry, Old Dominion University, Norfolk, Virginia 23529, USA.
⁷ Department of Biological Sciences, University of New Orleans, New Orleans, Louisiana 70148, USA.
⁸ U.S. Geological Survey, Western Fisheries Research Center, Seattle, Washington 98115, USA.
⁹ University of Washington, Dept. of Environmental and Occupational Health Sciences, School of Public Health, Seattle, Washington 98105, USA.
¹⁰ Department of Chemistry, Chemical Analysis & Mass Spectrometry Facility, University of New Orleans, New Orleans, Louisiana 70148, USA; Department of Chemistry, University of Alaska Anchorage, Anchorage, AK 99508, USA.
¹¹ Department of Chemistry, Chemical Analysis & Mass Spectrometry Facility, University of New Orleans, New Orleans, Louisiana 70148, USA; Pontchartrain Institute for Environmental Sciences, Shea Penland Coastal Education & Research Facility, University of New Orleans, New Orleans, Louisiana 70148, USA; Department of Chemistry, University of Alaska Anchorage, Anchorage, AK 99508, USA. Electronic address: dcpodgor@uno.edu.

PMID: 39521076
DOI: 10.1016/j.scitotenv.2024.177447

Abstract

Crude oil toxicity to early life stage fish is commonly attributed to polycyclic aromatic hydrocarbons (PAHs). However, it remains unclear how the polar unresolved complex mixture (UCM), which constitutes the bulk of the water-soluble fraction of crude oil, contributes to crude oil toxicity. Additionally, the role of photomodification-induced toxicity in relation to the polar UCM is not well understood. This study addresses these knowledge gaps by assessing the toxicity of two laboratory generated polar UCMs from Cook Inlet crude oil, representing the readily water-soluble fraction of crude oil and photoproduced hydrocarbon oxidation products (HOPs), to Pacific herring (Clupea pallasii) embryos. A small-scale semi-static exposure design was utilized with a range of polar UCM concentrations (0.5-14 mg/L) in nonvolatile dissolved organic carbon (NVDOC) units, quantifying the entire polar UCM. Compositional analyses revealed a photochemical-driven shift toward more complex aromatic compositions, naphthenic acids, and no detectable levels of PAHs (above 0.3 μg/L). Exposure to the dark polar UCM resulted in higher mortality than exposure to the light polar UCM. Both dark and light polar UCMs induced developmental abnormalities commonly attributed to the PAH fraction, including edema, reduced heart rate, body axis defects, and decreased body lengths, with these effects observed at the lowest dose group (0.5 mg/L NVDOC). These responses suggest photomodification-induced toxicity is driven by exposure to increased concentrations of dissolved HOPs rather than photochemical induced compositional changes. Gene expression analyses focusing on xenobiotic metabolism and cardiac morphogenesis yielded results consistent with previous studies examining the biological mechanisms of crude oil toxicity. In summary, these phenotypic and genotypic responses in Pacific herring embryos indicate that the polar UCM is a significant driver of crude oil toxicity. These findings emphasize the importance of considering the polar UCM in future studies, metric reporting, and risk assessments related to crude oil toxicity.

Keywords: Cardiotoxicity; Early life stage fish; Ecotoxicology; Oil spills; Photo-enhanced toxicity; Unresolved complex mixture (UCM).