Dataset Information

AHR-related activities in a creosote-adapted population of adult atlantic killifish, Fundulus heteroclitus, two decades post-EPA superfund status at the Atlantic Wood Site, Portsmouth, VA USA.

ABSTRACT: Atlantic killifish, Fundulus heteroclitus, are adapted to creosote-based PAHs at the US EPA Superfund site known as Atlantic Wood (AW) on the southern branch of the Elizabeth River, VA USA. Subsequent to the discovery of the AW population in the early 1990s, these fish were shown to be recalcitrant to CYP1A induction by PAHs under experimental conditions, and even to the time of this study, killifish embryos collected from the AW site are resistant to developmental deformities typically associated with exposure to PAHs in reference fish. Historically, however, 90 +% of the adult killifish at this site have proliferative hepatic lesions including cancer of varying severity. Several PAHs at this site are known to be ligands for the aryl hydrocarbon receptor (AHR). In this study, AHR-related activities in AW fish collected between 2011 and 2013 were re-examined nearly 2 decades after first discovery. This study shows that CYP1A mRNA expression is three-fold higher in intestines of AW killifish compared to a reference population. Using immunohistochemistry, CYP1A staining in intestines was uniformly positive compared to negative staining in reference fish. Livers of AW killifish were examined by IHC to show that CYP1A and AHR2 protein expression reflect lesions-specific patterns, probably representing differences in intrinsic cellular physiology of the spectrum of proliferative lesions comprising the hepatocarcinogenic process. We also found that COX2 mRNA expression levels were higher in AW fish livers compared to those in the reference population, suggesting a state of chronic inflammation. Overall, these findings suggest that adult AW fish are responsive to AHR signaling, and do express CYP1A and AHR2 proteins in intestines at a level above what was observed in the reference population.

SUBMITTER: Wojdylo JV

PROVIDER: S-EPMC4967385 | biostudies-literature | 2016 Aug

REPOSITORIES: biostudies-literature

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AHR-related activities in a creosote-adapted population of adult atlantic killifish, Fundulus heteroclitus, two decades post-EPA superfund status at the Atlantic Wood Site, Portsmouth, VA USA.

Wojdylo Josephine V JV Vogelbein Wolfgang W Bain Lisa J LJ Rice Charles D CD

Aquatic toxicology (Amsterdam, Netherlands) 20160522

Atlantic killifish, Fundulus heteroclitus, are adapted to creosote-based PAHs at the US EPA Superfund site known as Atlantic Wood (AW) on the southern branch of the Elizabeth River, VA USA. Subsequent to the discovery of the AW population in the early 1990s, these fish were shown to be recalcitrant to CYP1A induction by PAHs under experimental conditions, and even to the time of this study, killifish embryos collected from the AW site are resistant to developmental deformities typically associat ...[more]

PMID: 27262937

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Project description:Fundulus heteroclitus (Atlantic killifish) found at the Atlantic Wood Industries Superfund site on the Elizabeth River (ER) in Portsmouth, VA (USA), have been shown to be resistant to the teratogenic effects of creosote-contaminated sediments found at this highly contaminated site. Many of the polycyclic aromatic hydrocarbons (PAHs) found at the ER are known to activate the aryl hydrocarbon receptor (AHR), and are thought to mediate their toxic effects through this pathway. Activation of the AHR results in the induction of several Phase I and II metabolic enzymes. It has been previously shown that the AHR of killifish from the ER are refractory to induction by AHR agonists. To more fully characterize this altered AHR response, we exposed embryos from the ER and from a reference site on King's Creek, VA (KC) to two PAHs, benzo[alpha]pyrene (BaP) and benzo[k]fluoranthene (BkF), and to the dioxin-like compound (DLC), 3,3',4,4',5-pentachlorobiphenyl (PCB126). We compared their developmental and molecular responses by screening the embryos for CYP1A enzyme activity, cardiac deformities, and mRNA expression of CYP1A, CYP1B1, CYP1C1, and AHR2. Basal gene expression of both CYP1A and CYP1B1 was 40% higher in the KC control embryos compared to those from the ER, while AHR2 and CYP1C1 were not significantly different between the populations. Exposure of KC embryos to BaP, BkF, and PCB126 induced CYP1A activity and cardiac deformities. In contrast, CYP1A activity was induced in ER embryos only in response to BkF exposure, although this induction in ER embryos was significantly lower than that observed in KC fish at comparable concentrations. ER embryos did not develop cardiac deformities in response to any of the chemicals tested. CYP1A, CYP1B1 and CYP1C1 mRNA were all significantly induced in the KC embryos after exposure to BaP, BkF and PCB126. Exposure to BaP and BkF in ER embryos resulted in a significant induction of CYP1A mRNA, albeit significantly lower than observed in KC fish. Interestingly, BaP exposure resulted in induction of CYP1B1 at comparable levels in embryos from both populations. CYP1s were not induced in ER embryos in response to PCB126, nor was CYP1C1 for any treatment examined. Additionally, AHR2 was not significantly induced for any of the treatment groups. This study further characterizes the AHR response in killifish, and provides greater insight into the adapted ER phenotype. The ER adaptation involves the suppression of normal AHR-inducible gene expression for all three CYP1 genes, and therefore is likely an alteration in AHR signaling or control.

Project description:The non-migratory killifish Fundulus heteroclitus inhabits clean and polluted environments interspersed throughout its range along the Atlantic coast of North America. Several populations of this species have successfully adapted to environments contaminated with toxic aromatic hydrocarbon pollutants such as polychlorinated biphenyls (PCBs). Previous studies suggest that the mechanism of resistance to these and other "dioxin-like compounds" (DLCs) may involve reduced signaling through the aryl hydrocarbon receptor (AHR) pathway. Here we investigated gene diversity and evidence for positive selection at three AHR-related loci (AHR1, AHR2, AHRR) in F. heteroclitus by comparing alleles from seven locations ranging over 600 km along the northeastern US, including extremely polluted and reference estuaries, with a focus on New Bedford Harbor (MA, USA), a PCB Superfund site, and nearby reference sites.We identified 98 single nucleotide polymorphisms within three AHR-related loci among all populations, including synonymous and nonsynonymous substitutions. Haplotype distributions were spatially segregated and F-statistics suggested strong population genetic structure at these loci, consistent with previous studies showing strong population genetic structure at other F. heteroclitus loci. Genetic diversity at these three loci was not significantly different in contaminated sites as compared to reference sites. However, for AHR2 the New Bedford Harbor population had significant FST values in comparison to the nearest reference populations. Tests for positive selection revealed ten nonsynonymous polymorphisms in AHR1 and four in AHR2. Four nonsynonymous SNPs in AHR1 and three in AHR2 showed large differences in base frequency between New Bedford Harbor and its reference site. Tests for isolation-by-distance revealed evidence for non-neutral change at the AHR2 locus.Together, these data suggest that F. heteroclitus populations in reference and polluted sites have similar genetic diversity, providing no evidence for strong genetic bottlenecks for populations in polluted locations. However, the data provide evidence for genetic differentiation among sites, selection at specific nucleotides in AHR1 and AHR2, and specific AHR2 SNPs and haplotypes that are associated with the PCB-resistant phenotype in the New Bedford Harbor population. The results suggest that AHRs, and especially AHR2, may be important, recurring targets for selection in local adaptation to dioxin-like aromatic hydrocarbon contaminants.

Dataset Information

AHR-related activities in a creosote-adapted population of adult atlantic killifish, Fundulus heteroclitus, two decades post-EPA superfund status at the Atlantic Wood Site, Portsmouth, VA USA.

Publications

AHR-related activities in a creosote-adapted population of adult atlantic killifish, Fundulus heteroclitus, two decades post-EPA superfund status at the Atlantic Wood Site, Portsmouth, VA USA.

Similar Datasets

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