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A complex mixture of polycyclic aromatic compounds causes embryotoxic, behavioral, and molecular effects in zebrafish larvae (Danio rerio), and in vitro bioassays
Örebro University, School of Science and Technology. (Man-Technology-Environment Research Centre (MTM))ORCID iD: 0000-0002-9945-6619
Örebro University, School of Science and Technology. (Man-Technology-Environment Research Centre (MTM))ORCID iD: 0000-0003-1404-3186
Örebro University, School of Science and Technology. (Man-Technology-Environment Research Centre (MTM))ORCID iD: 0000-0002-4382-4355
Örebro University, School of Science and Technology.ORCID iD: 0000-0002-2356-6686
2024 (English)In: Science of the Total Environment, ISSN 0048-9697, E-ISSN 1879-1026, Vol. 906, article id 167307Article in journal (Refereed) Published
Abstract [en]

Polycyclic aromatic compounds (PACs) are prevalent in the environment, typically found in complex mixtures and high concentrations. Our understanding of the effects of PACs, excluding the 16 priority polycyclic aromatic hydrocarbons (16 PAHs), remains limited. Zebrafish embryos and in vitro bioassays were utilized to investigate the embryotoxic, behavioral, and molecular effects of a soil sample from a former gasworks site in Sweden. Additionally, targeted chemical analysis was conducted to analyze 87 PACs in the soil, fish, water, and plate material. CALUX® assays were used to assess the activation of aryl hydrocarbon and estrogen receptors, as well as the inhibition of the androgen receptor. Larval behavior was measured by analyzing activity during light and darkness and in response to mechanical stimulation. Furthermore, qPCR analyses were performed on a subset of 36 genes associated with specific adverse outcomes, and the total lipid content in the larvae was measured. Exposure to the sample resulted in embryotoxic effects (LC50 = 0.480 mg dry matter soil/mL water). The mixture also induced hyperactivity in darkness and hypoactivity in light and in response to the mechanical stimulus. qPCR analysis revealed differential regulation of 15 genes, including downregulation of opn1sw1 (eye pigmentation) and upregulation of fpgs (heart failure). The sample caused significant responses in three bioassays (ERα-, DR-, and PAH-CALUX), and the exposed larvae exhibited elevated lipid levels. Chemical analysis identified benzo[a]pyrene as the predominant compound in the soil and approximately half of the total PAC concentration was attributed to the 16 PAHs. This study highlights the value of combining in vitro and in vivo methods with chemical analysis to assess toxic mechanisms at specific targets and to elucidate the possible interactions between various pathways in an organism. It also enhances our understanding of the risks associated with environmental mixtures of PACs and their distribution during toxicity testing.

Place, publisher, year, edition, pages
Elsevier, 2024. Vol. 906, article id 167307
Keywords [en]
Chemical analysis, Environment, Gasworks, Lipidomics, Quantitative gene expression, Soil
National Category
Environmental Sciences
Identifiers
URN: urn:nbn:se:oru:diva-108825DOI: 10.1016/j.scitotenv.2023.167307ISI: 001102592900001PubMedID: 37804991Scopus ID: 2-s2.0-85173583428OAI: oai:DiVA.org:oru-108825DiVA, id: diva2:1803810
Funder
Knowledge Foundation, 201660019Available from: 2023-10-10 Created: 2023-10-10 Last updated: 2023-12-15Bibliographically approved
In thesis
1. Molecular and phenotypical toxicological effects of environmental pollutants and their mixtures: A mechanistic approach
Open this publication in new window or tab >>Molecular and phenotypical toxicological effects of environmental pollutants and their mixtures: A mechanistic approach
2023 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Current environmental risk assessment of polluted sites primarily relies on single compound evaluation. However, in the environment, organisms are often exposed to complex mixtures of pollutants. To further develop risk assessment of polluted sites and evaluate the risks that mixtures pose to humans and wildlife, a mechanistic understanding of mixture toxicity is needed.

The overall aim of this thesis was to increase our knowledge of the toxic effects caused by chemical mixtures and to develop new approaches to investigate the molecular mechanisms underlying such effects. To reach this aim, a comprehensive set of methods was applied, considering molecular and phenotypical alterations as well as chemical analyses.

The investigations revealed that the acute toxicity caused by mixtures of the pollutants B[a]P, PFOS, PCB126, and Arsenate is mainly predictable by concentration addition. The results also showed some specific sublethal effects of the various mixtures that were not observed for the single components. In addition, each mixture caused very specific patterns of behavioral alterations, gene expression changes, altered lipid content, and altered organ growth. A complex environmental mixture from soil contaminated with PACs caused for instance behavioral alterations in zebrafish, in addition to dysfunction of genes that are critical for eye development.

In summary, this thesis contributes to an increased understanding of the mechanistic pathways underlying the mixture toxicity of selected pollutants and environmental samples. In addition, it provides insights for the development of new approaches that may be included in risk assessment, such as image analysis and effect-directed analysis.

Place, publisher, year, edition, pages
Örebro: Örebro University, 2023. p. 89
Series
Örebro Studies in Environmental Science, ISSN 1650-6278 ; 19
Keywords
Environmental pollutants, mixtures, soil, zebrafish, Danio rerio, behavior, gene expression, lipidomics, image analysis, PCB126, PFOS, B[a]P, Arsenic, risk assessment
National Category
Other Biological Topics
Identifiers
urn:nbn:se:oru:diva-109438 (URN)9789175295282 (ISBN)9789175295299 (ISBN)
Public defence
2023-11-24, Örebro universitet, Forumhuset, Hörsal F, Fakultetsgatan 1, Örebro, 13:00 (Swedish)
Opponent
Supervisors
Available from: 2023-10-27 Created: 2023-10-27 Last updated: 2023-11-24Bibliographically approved

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Nilén, GretaLarsson, MariaHyötyläinen, TuuliaKeiter, Steffen

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