Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis Embryos
Naphthenic acids (NAs) are oil-derived mixtures of carboxylic acids and are considered emerging contaminants with the potential to disrupt development of aquatic species. In the Oil Sands Region of Canada, NAs are components of the water released following processing of the bitumen-containing sand....
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-08-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fmars.2019.00533/full |
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| author | Juan Manuel Gutierrez-Villagomez Christopher J. Martyniuk Lei Xing Valerie S. Langlois Bruce D. Pauli Jules M. Blais Vance L. Trudeau |
| author_facet | Juan Manuel Gutierrez-Villagomez Christopher J. Martyniuk Lei Xing Valerie S. Langlois Bruce D. Pauli Jules M. Blais Vance L. Trudeau |
| author_sort | Juan Manuel Gutierrez-Villagomez |
| collection | DOAJ |
| description | Naphthenic acids (NAs) are oil-derived mixtures of carboxylic acids and are considered emerging contaminants with the potential to disrupt development of aquatic species. In the Oil Sands Region of Canada, NAs are components of the water released following processing of the bitumen-containing sand. The aim of this research was to identify potential mechanisms of toxicity of NA mixtures. Silurana (Xenopus) tropicalis embryos were raised in water spiked with commercial oil-derived NA extracts (S1 and S2) at a sub-lethal concentration (2 mg/L). The transcriptomic responses of the whole 4-day old embryos following exposure were assessed using a custom oligonucleotide microarray. Both NA mixtures induced embryonic abnormalities that included edema, and cardiac and gut abnormalities. Exposure to NAs also affected morphometric parameters and decreased total length, tail length, and interorbital distance of the embryos. Gene ontology analysis revealed that 18 biological processes, 5 cellular components, and 19 molecular functions were significantly enriched after both S1 and S2 exposures. Sub-network enrichment analysis revealed pathways that were related to phenotypic abnormalities; these included gut function, edema, and cartilage differentiation. Other notable networks affected by NAs included metabolism and cell membrane integrity. In a separate dose-response experiment, the expression of key genes identified by microarray (cyp4b1, abcg2, slc26a6, eprs, and slc5a1) was determined by Real-Time qPCR in S. tropicalis embryos exposed to the commercial NAs and to acid-extractable organics (AEOs) prepared from Oil Sands Process-Affected Water. In general, the RT-qPCR data agreed with the microarray data. In S. tropicalis embryos exposed to the AEOs, the mRNA levels of eprs (bifunctional glutamate/proline-tRNA ligase) and slcs5a1 (sodium/glucose cotransporter 1) were significantly decreased compared to the controls. Such changes are likely indicative of increased edema and disrupted gut function, respectively. These data suggest that NAs have multiple modes of action to induce developmental toxicity in amphibians. Some modes of action may be shared between commercial NAs and AEOs. |
| first_indexed | 2024-12-11T12:37:43Z |
| format | Article |
| id | doaj.art-fface240dc41418d8068775ce33b8599 |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-12-11T12:37:43Z |
| publishDate | 2019-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-fface240dc41418d8068775ce33b85992022-12-22T01:07:04ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452019-08-01610.3389/fmars.2019.00533461397Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis EmbryosJuan Manuel Gutierrez-Villagomez0Christopher J. Martyniuk1Lei Xing2Valerie S. Langlois3Bruce D. Pauli4Jules M. Blais5Vance L. Trudeau6Department of Biology, University of Ottawa, Ottawa, ON, CanadaDepartment of Physiological Sciences and Center for Environmental and Human Toxicology, College of Veterinary Medicine, UF Genetics Institute, University of Florida, Gainesville, FL, United StatesDepartment of Biology, University of Ottawa, Ottawa, ON, CanadaInstitut National de la Recherche Scientifique, Centre Eau Terre Environnement, Quebec City, QC, CanadaEcotoxicology and Wildlife Health Division, Wildlife and Landscape Science Directorate, Science and Technology Branch, Environment and Climate Change Canada, Ottawa, ON, CanadaDepartment of Biology, University of Ottawa, Ottawa, ON, CanadaDepartment of Biology, University of Ottawa, Ottawa, ON, CanadaNaphthenic acids (NAs) are oil-derived mixtures of carboxylic acids and are considered emerging contaminants with the potential to disrupt development of aquatic species. In the Oil Sands Region of Canada, NAs are components of the water released following processing of the bitumen-containing sand. The aim of this research was to identify potential mechanisms of toxicity of NA mixtures. Silurana (Xenopus) tropicalis embryos were raised in water spiked with commercial oil-derived NA extracts (S1 and S2) at a sub-lethal concentration (2 mg/L). The transcriptomic responses of the whole 4-day old embryos following exposure were assessed using a custom oligonucleotide microarray. Both NA mixtures induced embryonic abnormalities that included edema, and cardiac and gut abnormalities. Exposure to NAs also affected morphometric parameters and decreased total length, tail length, and interorbital distance of the embryos. Gene ontology analysis revealed that 18 biological processes, 5 cellular components, and 19 molecular functions were significantly enriched after both S1 and S2 exposures. Sub-network enrichment analysis revealed pathways that were related to phenotypic abnormalities; these included gut function, edema, and cartilage differentiation. Other notable networks affected by NAs included metabolism and cell membrane integrity. In a separate dose-response experiment, the expression of key genes identified by microarray (cyp4b1, abcg2, slc26a6, eprs, and slc5a1) was determined by Real-Time qPCR in S. tropicalis embryos exposed to the commercial NAs and to acid-extractable organics (AEOs) prepared from Oil Sands Process-Affected Water. In general, the RT-qPCR data agreed with the microarray data. In S. tropicalis embryos exposed to the AEOs, the mRNA levels of eprs (bifunctional glutamate/proline-tRNA ligase) and slcs5a1 (sodium/glucose cotransporter 1) were significantly decreased compared to the controls. Such changes are likely indicative of increased edema and disrupted gut function, respectively. These data suggest that NAs have multiple modes of action to induce developmental toxicity in amphibians. Some modes of action may be shared between commercial NAs and AEOs.https://www.frontiersin.org/article/10.3389/fmars.2019.00533/fullacid extractable organicsedemagut abnormalitiesnaphthenic acidsoil sandsmicroarray |
| spellingShingle | Juan Manuel Gutierrez-Villagomez Christopher J. Martyniuk Lei Xing Valerie S. Langlois Bruce D. Pauli Jules M. Blais Vance L. Trudeau Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis Embryos Frontiers in Marine Science acid extractable organics edema gut abnormalities naphthenic acids oil sands microarray |
| title | Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis Embryos |
| title_full | Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis Embryos |
| title_fullStr | Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis Embryos |
| title_full_unstemmed | Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis Embryos |
| title_short | Transcriptome Analysis Reveals That Naphthenic Acids Perturb Gene Networks Related to Metabolic Processes, Membrane Integrity, and Gut Function in Silurana (Xenopus) tropicalis Embryos |
| title_sort | transcriptome analysis reveals that naphthenic acids perturb gene networks related to metabolic processes membrane integrity and gut function in silurana xenopus tropicalis embryos |
| topic | acid extractable organics edema gut abnormalities naphthenic acids oil sands microarray |
| url | https://www.frontiersin.org/article/10.3389/fmars.2019.00533/full |
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