Differential DNA methylation and metabolite profiling of Atlantic killifish (Fundulus heteroclitus) from the New Bedford Harbor Superfund site

Kim, Jiwan; Jung, Dawoon; Chatterjee, Nivedita; Clark, Bryan; Nacci, Diane; Kim, Suhkmann; Choi, Jinhee

doi:10.1007/s10646-023-02724-w

Differential DNA methylation and metabolite profiling of Atlantic killifish (Fundulus heteroclitus) from the New Bedford Harbor Superfund site

Journal Article · Fri Jan 05 23:00:00 EST 2024 · Ecotoxicology

DOI:https://doi.org/10.1007/s10646-023-02724-w· OSTI ID:2471334

Kim, Jiwan ^[1]; Jung, Dawoon ^[2]; Chatterjee, Nivedita ^[3]; Clark, Bryan ^[4]; Nacci, Diane ^[4]; Kim, Suhkmann ^[5]; ^[1]

University of Seoul (Korea, Republic of)
Korea Environment Institute (Korea, Republic of)
University of Seoul (Korea, Republic of); International Iberian Nanotechnology Laboratory (INL), Braga (Portugal)
US Environmental Protection Agency USEPA), Narragansett, RI (United States). Center for Environmental Measurement and Modeling
Pusan National Univ., Busan (Korea, Republic of)

Atlantic killifish (Fundulus heteroclitus) is a valuable model in evolutionary toxicology to study how the interactions between genetic and environmental factors serve the adaptive ability of organisms to resist chemical pollution. Killifish populations inhabiting environmental toxicant-contaminated New Bedford Harbor (NBH) show phenotypes tolerant to polychlorinated biphenyls (PCBs) and differences at the transcriptional and genomic levels. However, limited research has explored epigenetic alterations and metabolic effects in NBH killifish. To identify the involvement of epigenetic and metabolic regulation in the adaptive response of killifish, we investigated tissue- and sex-specific differences in global DNA methylation and metabolomic profiles of NBH killifish populations, compared to sensitive populations from a non-polluted site, Scorton Creek (SC). The results revealed that liver-specific global DNA hypomethylation and differential metabolites were evident in fish from NBH compared with those from SC. The sex-specific differences were not greater than the tissue-specific differences. We demonstrated liver-specific enriched metabolic pathways (e.g., amino acid metabolic pathways converged into the urea cycle and glutathione metabolism), suggesting possible crosstalk between differential metabolites and DNA hypomethylation in the livers of NBH killifish. Additional investigation of methylated gene regions is necessary to understand the functional role of DNA hypomethylation in the regulation of enzyme-encoding genes associated with metabolic processes and physiological changes in NBH populations.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge Institute for Science and Education (ORISE), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USEPA; National Research Foundation of Korea

Grant/Contract Number:: SC0014664

OSTI ID:: 2471334

Journal Information:: Ecotoxicology, Journal Name: Ecotoxicology Journal Issue: 1 Vol. 33; ISSN 0963-9292

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (40)

Predicting the occurrence of genetic adaptation to dioxinlike compounds in populations of the estuarine fish Fundulus heteroclitus Nacci, Diane E.; Champlin, Denise; Coiro, Laura Environmental Toxicology and Chemistry, Vol. 21, Issue 7 https://doi.org/10.1002/etc.5620210726	journal	July 2002
Adaptations of wild populations of the estuarine fish Fundulus heteroclitus to persistent environmental contaminants Nacci, D.; Coiro, L.; Champlin, D. Marine Biology, Vol. 134, Issue 1 https://doi.org/10.1007/s002270050520	journal	June 1999
Environmental Monitoring Of Remedial Dredging At The New Bedford Harbor, Ma, Superfund Site Bergen, Barbara J.; Nelson, William G.; Mackay, Joseph Environmental Monitoring and Assessment, Vol. 111, Issue 1-3 https://doi.org/10.1007/s10661-005-8223-4	journal	December 2005
The New Bedford Harbor Superfund site long-term monitoring program (1993–2009) Nelson, William G.; Bergen, Barbara J. Environmental Monitoring and Assessment, Vol. 184, Issue 12 https://doi.org/10.1007/s10661-012-2517-0	journal	January 2012
Effects of heavy metals (Cd, Cu, Cr, Pb, Zn) on fish glutathione metabolism Eroglu, A.; Dogan, Z.; Kanak, E. G. Environmental Science and Pollution Research, Vol. 22, Issue 5 https://doi.org/10.1007/s11356-014-2972-y	journal	May 2014
Adaptation of the Estuarine Fish Fundulus heteroclitus (Atlantic Killifish) to Polychlorinated Biphenyls (PCBs) Nacci, Diane E.; Champlin, Denise; Jayaraman, Saro Estuaries and Coasts, Vol. 33, Issue 4 https://doi.org/10.1007/s12237-009-9257-6	journal	January 2010
An overview of toxicant identification in sediments and dredged materials Ho, Kay T.; Burgess, Robert M.; Pelletier, Marguerite C. Marine Pollution Bulletin, Vol. 44, Issue 4 https://doi.org/10.1016/S0025-326X(01)00251-X	journal	April 2002
How myo-inositol improves the physiological functions of aquatic animals: A review Cui, Wenxiao; Ma, Aijun; Farhadi, Ardavan Aquaculture, Vol. 553 https://doi.org/10.1016/j.aquaculture.2022.738118	journal	May 2022
Role of DNA methylation of AHR1 and AHR2 promoters in differential sensitivity to PCBs in Atlantic Killifish, Fundulus heteroclitus Aluru, Neelakanteswar; Karchner, Sibel I.; Hahn, Mark E. Aquatic Toxicology, Vol. 101, Issue 1 https://doi.org/10.1016/j.aquatox.2010.10.010	journal	January 2011
Copper exposure induces oxidative injury, disturbs the antioxidant system and changes the Nrf2/ARE (CuZnSOD) signaling in the fish brain: Protective effects of myo-inositol Jiang, Wei-Dan; Liu, Yang; Hu, Kai Aquatic Toxicology, Vol. 155 https://doi.org/10.1016/j.aquatox.2014.07.003	journal	October 2014
Regulation of pregnane-X-receptor, CYP3A and P-glycoprotein genes in the PCB-resistant killifish (Fundulus heteroclitus) population from New Bedford Harbor Gräns, Johanna; Wassmur, Britt; Fernández-Santoscoy, María Aquatic Toxicology, Vol. 159 https://doi.org/10.1016/j.aquatox.2014.12.010	journal	February 2015
Expression and function of ryanodine receptor related pathways in PCB tolerant Atlantic killifish (Fundulus heteroclitus) from New Bedford Harbor, MA, USA Fritsch, Erika B.; Stegeman, John J.; Goldstone, Jared V. Aquatic Toxicology, Vol. 159 https://doi.org/10.1016/j.aquatox.2014.12.017	journal	February 2015
Genome-wide scan reveals signatures of selection related to pollution adaptation in non-model estuarine Atlantic killifish (Fundulus heteroclitus) Osterberg, J. S.; Cammen, K. M.; Schultz, T. F. Aquatic Toxicology, Vol. 200 https://doi.org/10.1016/j.aquatox.2018.04.017	journal	July 2018
Hepatic metabolite profiling of polychlorinated biphenyl (PCB)-resistant and sensitive populations of Atlantic killifish (Fundulus heteroclitus) Glazer, Lilah; Kido Soule, Melissa C.; Longnecker, Krista Aquatic Toxicology, Vol. 205 https://doi.org/10.1016/j.aquatox.2018.10.007	journal	December 2018
Transcriptomic and physiological analysis of endocrine disrupting chemicals Impacts on 3D Zebrafish liver cell culture system Park, Chang Gyun; Ryu, Chang Seon; Sung, Baeckkyoung Aquatic Toxicology, Vol. 245 https://doi.org/10.1016/j.aquatox.2022.106105	journal	April 2022
Analysis of CpG methylation in the killifish CYP1A promoter Timme-Laragy, Alicia R.; Meyer, Joel N.; Waterland, Robert A. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, Vol. 141, Issue 4 https://doi.org/10.1016/j.cbpc.2005.09.009	journal	August 2005
Oxidative stress biomarkers in the freshwater characid fish, Brycon cephalus, exposed to organophosphorus insecticide Folisuper 600 (methyl parathion) Monteiro, Diana Amaral; de Almeida, Jeane Alves; Rantin, Francisco Tadeu Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, Vol. 143, Issue 2 https://doi.org/10.1016/j.cbpc.2006.01.004	journal	June 2006
Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes Masella, Roberta; Di Benedetto, Roberta; Varì, Rosaria The Journal of Nutritional Biochemistry, Vol. 16, Issue 10 https://doi.org/10.1016/j.jnutbio.2005.05.013	journal	October 2005
Application of integrated transcriptomic, proteomic and metabolomic profiling for the delineation of mechanisms of drug induced cell stress Wilmes, Anja; Limonciel, Alice; Aschauer, Lydia Journal of Proteomics, Vol. 79 https://doi.org/10.1016/j.jprot.2012.11.022	journal	February 2013
Oxidative stress in two populations of killifish (Fundulus heteroclitus) with differing contaminant exposure histories Bacanskas, Lisa R.; Whitaker, Julia; Di Giulio, Richard T. Marine Environmental Research, Vol. 58, Issue 2-5 https://doi.org/10.1016/j.marenvres.2004.03.048	journal	August 2004
CYP1B1 knockdown does not alter synergistic developmental toxicity of polycyclic aromatic hydrocarbons in zebrafish (Danio rerio) Timme-Laragy, Alicia R.; Noyes, Pamela D.; Buhler, Donald R. Marine Environmental Research, Vol. 66, Issue 1 https://doi.org/10.1016/j.marenvres.2008.02.030	journal	July 2008
Multi-omics responses in tree swallow (Tachycineta bicolor) nestlings from the Maumee Area of Concern, Maumee River, Ohio Tseng, Chi Yen; Custer, Christine M.; Custer, Thomas W. Science of The Total Environment, Vol. 856 https://doi.org/10.1016/j.scitotenv.2022.159130	journal	January 2023
An elevated glutathione S-transferase in creosote-resistant mummichog (Fundulus heteroclitus) Armknecht, Susan L.; Kaattari, Stephen L.; Van Veld, Peter A. Aquatic Toxicology, Vol. 41, Issue 1-2 https://doi.org/10.1016/s0166-445x(97)00074-x	journal	March 1998
Evaluation of Pressurized Fluid Extraction for the Extraction of Environmental Matrix Reference Materials Schantz, Michele M.; Nichols, John J.; Wise, Stephen A. Analytical Chemistry, Vol. 69, Issue 20 https://doi.org/10.1021/ac970299c	journal	October 1997
Urea excretion as a strategy for survival in a fish living in a very alkaline environment Randall, D. J.; Wood, C. M.; Perry, S. F. Nature, Vol. 337, Issue 6203 https://doi.org/10.1038/337165a0	journal	January 1989
Integrative analysis of 111 reference human epigenomes Kundaje, Anshul; Meuleman, Wouter; Ernst, Jason Nature, Vol. 518, Issue 7539 https://doi.org/10.1038/nature14248	journal	February 2015
Epigenetics meets metabolomics: an epigenome-wide association study with blood serum metabolic traits Petersen, Ann-Kristin; Zeilinger, Sonja; Kastenmüller, Gabi Human Molecular Genetics, Vol. 23, Issue 2 https://doi.org/10.1093/hmg/ddt430	journal	September 2013
Acquired Resistance to Ah Receptor Agonists in a Population of Atlantic Killifish (Fundulus heteroclitus) Inhabiting a Marine Superfund Site: In Vivo and in Vitro Studies on the Inducibility of Xenobiotic Metabolizing Enzymes Bello, S. M.; Franks, D. G.; Stegeman, J. J. Toxicological Sciences, Vol. 60, Issue 1 https://doi.org/10.1093/toxsci/60.1.77	journal	March 2001
Aryl hydrocarbon receptor polymorphisms and dioxin resistance in Atlantic killifish (Fundulus heteroclitus) Hahn, Mark E.; Karchner, Sibel I.; Franks, Diana G. Pharmacogenetics, Vol. 14, Issue 2 https://doi.org/10.1097/00008571-200402000-00007	journal	January 2004
How does epigenetics influence the course of evolution? Ashe, Alyson; Colot, Vincent; Oldroyd, Benjamin P. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 376, Issue 1826 https://doi.org/10.1098/rstb.2020.0111	journal	April 2021
When evolution is the solution to pollution: Key principles, and lessons from rapid repeated adaptation of killifish ( Fundulus heteroclitus ) populations Whitehead, Andrew; Clark, Bryan W.; Reid, Noah M. Evolutionary Applications, Vol. 10, Issue 8 https://doi.org/10.1111/eva.12470	journal	April 2017
Tissue-specific dysregulation of DNA methylation in aging: Tissue-specific epigenetic dysregulation with aging Thompson, Reid F.; Atzmon, Gil; Gheorghe, Ciprian Aging Cell, Vol. 9, Issue 4 https://doi.org/10.1111/j.1474-9726.2010.00577.x	journal	May 2010
Genetic basis for rapidly evolved tolerance in the wild: adaptation to toxic pollutants by an estuarine fish species Nacci, Diane; Proestou, Dina; Champlin, Denise Molecular Ecology, Vol. 25, Issue 21 https://doi.org/10.1111/mec.13848	journal	October 2016
The genomic landscape of rapid repeated evolutionary adaptation to toxic pollution in wild fish Reid, N. M.; Proestou, D. A.; Clark, B. W. Science, Vol. 354, Issue 6317 https://doi.org/10.1126/science.aah4993	journal	December 2016
Environmental epigenetics in zebrafish Cavalieri, Vincenzo; Spinelli, Giovanni Epigenetics & Chromatin, Vol. 10, Issue 1 https://doi.org/10.1186/s13072-017-0154-0	journal	October 2017
Genetics Meets Metabolomics: A Genome-Wide Association Study of Metabolite Profiles in Human Serum Gieger, Christian; Geistlinger, Ludwig; Altmaier, Elisabeth PLoS Genetics, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pgen.1000282	journal	November 2008
Heritable Adaptation and Fitness Costs in Killifish (Fundulus Heteroclitus) Inhabiting a Polluted Estuary Meyer, Joel N.; Di Giulio, Richard T. Ecological Applications, Vol. 13, Issue 2 https://doi.org/10.1890/1051-0761(2003)013[0490:HAAFCI]2.0.CO;2	journal	April 2003
Identification of Acute Toxicants in new Bedford Harbor Sediments Ho, Kay T.; McKinney, Richard A.; Kuhn, Anne Environmental Toxicology and Chemistry, Vol. 16, Issue 3 https://doi.org/10.1897/1551-5028(1997)016<0551:IOATIN>2.3.CO;2	journal	January 1997
Ammonia in Aquatic Systems Francis-Floyd, Ruth; Watson, Craig; Petty, Denise EDIS, Vol. 2022, Issue 4 https://doi.org/10.32473/edis-fa031-2022	journal	July 2022
Integrated Metabolomics-DNA Methylation Analysis Reveals Significant Long-Term Tissue-Dependent Directional Alterations in Aminoacyl-tRNA Biosynthesis in the Left Ventricle of the Heart and Hippocampus Following Proton Irradiation Torres, Eileen Ruth S.; Hall, Reed; Bobe, Gerd Frontiers in Molecular Biosciences, Vol. 6 https://doi.org/10.3389/fmolb.2019.00077	journal	September 2019

Figures / Tables (6)

Similar Records

Extraintestinal calcium uptake in the killifish, Fundulus heteroclitus

Journal Article · Thu Sep 01 00:00:00 EDT 1983 · J. Exp. Zool.; (United States) · OSTI ID:6748077

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
54 ENVIRONMENTAL SCIENCES
Atlantic killifish
DNA methylation
Environmental Sciences & Ecology
Metabolomics
New Bedford Harbor Superfund site
Tissue-specific
Toxicology

Differential DNA methylation and metabolite profiling of Atlantic killifish (Fundulus heteroclitus) from the New Bedford Harbor Superfund site

Citation Formats

References (40)

Figures / Tables (6)

Similar Records

Related Subjects