History of exposure to copper influences transgenerational gene expression responses in Daphnia magna

References

• Carpenter SR, Stanley EH, Vander Zanden MJ. State of the world’s freshwater ecosystems: physical, chemical, and biological changes. Annu Rev Environ Resour. 2011;36(1):75–15. doi: 10.1146/annurev-environ-021810-094524
   Web of Science ®Google Scholar
• Gardner RC, Finlayson C. Global wetland outlook: state of the world’s wetlands and their services to people, Ramsar convention secretariat. Florida, US: Secretariat of the Ramsar Convention; 2018.
   Google Scholar
• Turak E, Harrison I, Dudgeon D, et al. Essential biodiversity variables for measuring change in global freshwater biodiversity. Biol Conserv. 2017;213:272–279. doi: 10.1016/j.biocon.2016.09.005
   Web of Science ®Google Scholar
• Ali H, Khan E, Ilahi I. Environmental chemistry and ecotoxicology of hazardous heavy metals: environmental persistence, toxicity, and bioaccumulation. J Chem. 2019;2019:1–14. doi: 10.1155/2019/6730305
   Web of Science ®Google Scholar
• Ali H, Khan E. Bioaccumulation of non-essential hazardous heavy metals and metalloids in freshwater fish. Risk to human health. Environ Chem Lett. 2018;16(3):903–917. doi: 10.1007/s10311-018-0734-7
   Web of Science ®Google Scholar
• Closs GP, Krkosek M, Olden JD. Conservation of freshwater fishes. United Kingdom: Cambridge University Press; 2016.
   Google Scholar
• Adams W, Blust R, Dwyer R, et al. Bioavailability assessment of metals in freshwater environments: a historical review. Environ Toxicol Chem. 2020;39(1):48–59. doi: 10.1002/etc.4558
   PubMed Web of Science ®Google Scholar
• Butcher J, Diamond J, Bearr J, et al. Toxicity models of pulsed copper exposure to Pimephales promelas and Daphnia magna. Environ Toxicol Chem. 2006;25(9):2541–2550. doi: 10.1897/05-630R.1
   PubMed Web of Science ®Google Scholar
• Venâncio C, Ribeiro R, Soares AMVM, et al. Survival recovery rates by six clonal lineages of daphnia longispina after intermittent exposures to copper. Chemosphere. 2021;264:128403. doi: 10.1016/j.chemosphere.2020.128403
   PubMed Web of Science ®Google Scholar
• Chain FJJ, Finlayson S, Crease T, et al. Variation in transcriptional responses to copper exposure across Daphnia pulex lineages. Aquat Toxicol. 2019;210:85–97. doi: 10.1016/j.aquatox.2019.02.016
   PubMed Web of Science ®Google Scholar
• Jansen M, De Meester L, Cielen A, et al. The interplay of past and current stress exposure on the water flea daphnia. Funct Ecol. 2011;25(5):974–982. doi: 10.1111/j.1365-2435.2011.01869.x
   Web of Science ®Google Scholar
• Schunck F, Liess M. Time between sequential exposures to multiple stress turns antagonism into synergism. Environ Sci Technol. 2022;56(20):14660–14667. doi: 10.1021/acs.est.2c04345
   PubMed Web of Science ®Google Scholar
• Abdullahi M, Zhou J, Dandhapani V, et al. Historical exposure to chemicals reduces tolerance to novel chemical stress in Daphnia (waterflea). Mol Ecol. 2022;31(11):3098–3111. doi: 10.1111/mec.16451
   PubMed Web of Science ®Google Scholar
• Poynton HC, Zuzow R, Loguinov AV, et al. Gene expression profiling in Daphnia magna, part II: validation of a copper specific gene expression signature with effluent from two copper mines in California. Environ Sci Technol. 2008b;42(16):6257–6263. doi: 10.1021/es800262k
   PubMed Web of Science ®Google Scholar
• Cuenca-Cambronero M, Pantel JH, Marshall H, et al. Evolutionary mechanisms underpinning fitness response to multiple stressors in Daphnia. Evol Appl. 2021;14(10):2457–2469. doi: 10.1111/eva.13258
   PubMed Web of Science ®Google Scholar
• Jeremias G, Barbosa J, Marques SM, et al. Transgenerational inheritance of DNA hypomethylation in Daphnia magna in response to salinity stress. Environ Sci Technol. 2018b;52:10114–10123. doi: 10.1021/acs.est.8b03225
   PubMed Web of Science ®Google Scholar
• Kimberly DA, Salice CJ. Multigenerational contaminant exposures produce non-monotonic, transgenerational responses in Daphnia magna. Environ Pollut. 2015;207:176–182. doi: 10.1016/j.envpol.2015.09.020
   PubMed Web of Science ®Google Scholar
• Shaw JR, Colbourne JK, Davey JC, et al. Gene response profiles for Daphnia pulex exposed to the environmental stressor cadmium reveals novel crustacean metallothioneins. BMC Genomics. 2007;8(1):477. doi: 10.1186/1471-2164-8-477
   PubMedGoogle Scholar
• Athanasio CG, Sommer U, Viant MR, et al. Use of 5-azacytidine in a proof-of-concept study to evaluate the impact of pre-natal and post-natal exposures, as well as within generation persistent DNA methylation changes in Daphnia. Ecotoxicology. 2018;27(5):556–568. doi: 10.1007/s10646-018-1927-3
   PubMed Web of Science ®Google Scholar
• Barata C, Campos B, Rivetti C, et al. Validation of a two-generational reproduction test in Daphnia magna: an interlaboratory exercise. Sci Total Environ. 2017;579:1073–1083. doi: 10.1016/j.scitotenv.2016.11.066
   PubMed Web of Science ®Google Scholar
• Neuparth T, Machado AM, Montes R, et al. Transgenerational inheritance of chemical-induced signature: a case study with simvastatin. Environ Int. 2020;144:106020. doi: 10.1016/j.envint.2020.106020
   PubMed Web of Science ®Google Scholar
• Yin J, Zhou M, Lin Z, et al. Transgenerational effects benefit offspring across diverse environments: a meta‐analysis in plants and animals. Ecol Lett. 2019;22(11):1976–1986. doi: 10.1111/ele.13373
   PubMed Web of Science ®Google Scholar
• Castro BB, Freches AR, Rodrigues M, et al. Transgenerational effects of toxicants: an extension of the daphnia 21-day chronic assay? Arch Environ Contam Toxicol. 2018;74(4):616–626. doi: 10.1007/s00244-018-0507-0
   PubMed Web of Science ®Google Scholar
• Shaw JLA, Judy JD, Kumar A, et al. Incorporating transgenerational epigenetic Inheritance into ecological risk assessment frameworks. Environ Sci Technol. 2017;51:9433–9445. doi: 10.1021/acs.est.7b01094
   PubMed Web of Science ®Google Scholar
• Burggren W. Epigenetic inheritance and its role in evolutionary biology: re-evaluation and new perspectives. Biology. 2016;5(2):24. doi: 10.3390/biology5020024
   PubMedGoogle Scholar
• Jeremias G, Barbosa J, Marques SM, et al. Synthesizing the role of epigenetics in the response and adaptation of species to climate change in freshwater ecosystems. Mol Ecol. 2018a;27(13):2790–2806. doi: 10.1111/mec.14727
   PubMed Web of Science ®Google Scholar
• Jeremias G, Gonçalves FJM, Asselman J, et al. Epigenetic regulation: the cross-talk among development, adaptive strategies, and microevolutionary change. In: Vaschetto LM, editor. Epigenetics, development, ecology and evolution. Springer; 2022a. pp. 5–33. doi: 10.1007/978-3-031-13771-6_2.
   Google Scholar
• Hanson MA, Skinner MK. Developmental origins of epigenetic transgenerational inheritance. Environ Epigenetics. 2016;2(1):1–9. doi: 10.1093/eep/dvw002
   Google Scholar
• Lindeman LC, Thaulow J, Song Y, et al. Epigenetic, transcriptional and phenotypic responses in two generations of Daphnia magna exposed to the DNA methylation inhibitor 5-azacytidine. Environ Epigenetics. 2019;5(3):1–12. doi: 10.1093/eep/dvz016
   Web of Science ®Google Scholar
• Harris KDM, Bartlett NJ, Lloyd VK. Daphnia as an emerging epigenetic model organism. Genet Res Int. 2012;2012:1–8. doi: 10.1155/2012/147892
   Google Scholar
• Kim HJ, Koedrith P, Seo YR. Ecotoxicogenomic approaches for understanding molecular mechanisms of environmental chemical toxicity using aquatic invertebrate, daphnia model organism. Int J Mol Sci. 2015;16(12):12261–12287. doi: 10.3390/ijms160612261
   PubMedGoogle Scholar
• Shaw JR, Pfrender ME, Eads BD, et al. Daphnia as an emerging model for toxicological genomics. Adv Exp Biol. 2008;2:165–219. doi: 10.1016/S1872-2423(08)00005-7
   Google Scholar
• Asselman J, Semmouri I, Jackson CE, et al. Genome-wide stress responses to copper and arsenic in a field population of Daphnia. Environ Sci Technol. 2019;53:3850–3859. doi: 10.1021/acs.est.8b06720
   PubMed Web of Science ®Google Scholar
• Jeremias G, Veloso T, Gonçalves FJM, et al. Multigenerational DNA methylation responses to copper exposure in Daphnia: potential targets for epigenetic biomarkers? Chemosphere. 2022b;308:136231. doi: 10.1016/j.chemosphere.2022.136231
   PubMed Web of Science ®Google Scholar
• Kvist J, Athanàsio CG, Pfrender ME, et al. A comprehensive epigenomic analysis of phenotypically distinguishable, genetically identical female and male Daphnia pulex. BMC Genomics. 2020;21(1):17. doi: 10.1186/s12864-019-6415-5
   PubMed Web of Science ®Google Scholar
• Vandegehuchte MB, De Coninck D, Vandenbrouck T, et al. Gene transcription profiles, global DNA methylation and potential transgenerational epigenetic effects related to zn exposure history in Daphnia magna. Environ Pollut. 2010a;158(10):3323–3329. doi: 10.1016/j.envpol.2010.07.023
   PubMed Web of Science ®Google Scholar
• Vandegehuchte MB, Vandenbrouck T, Coninck DD, et al. Can metal stress induce transferable changes in gene transcription in Daphnia magna? Aquat Toxicol. 2010c;97(3):188–195. doi: 10.1016/j.aquatox.2009.07.013
   PubMed Web of Science ®Google Scholar
• Bell AM, Stein LR. Transgenerational and developmental plasticity at the molecular level: lessons from Daphnia. Mol Ecol. 2017;26(19):4859–4861. doi: 10.1111/mec.14327
   PubMed Web of Science ®Google Scholar
• Kovalchuk I. Transgenerational epigenetic inheritance in animals. Front Genet. 2012;3. doi: 10.3389/fgene.2012.00076
   PubMedGoogle Scholar
• Skinner MK. What is an Epigenetic Transgenerational Phenotype? F3 or F2. Reprod Toxicol. 2008;25(1):2–6. doi: 10.1016/j.reprotox.2007.09.001
   PubMed Web of Science ®Google Scholar
• Jeremias G, Gonçalves FJM, Pereira JL, et al. Prospects for incorporation of epigenetic biomarkers in human health and environmental risk assessment of chemicals. Biol Rev. 2020;95(3):822–846. doi: 10.1111/brv.12589
   PubMed Web of Science ®Google Scholar
• Poynton HC, Loguinov AV, Varshavsky JR, et al. Gene expression profiling in Daphnia magna part I: concentration-dependent profiles provide support for the no observed transcriptional effect level. Environ Sci Technol. 2008a;42(16):6250–6256. doi: 10.1021/es8010783
   PubMed Web of Science ®Google Scholar
• Ray PD, Yosim A, Fry RC. Incorporating epigenetic data into the risk assessment process for the toxic metals arsenic, cadmium, chromium, lead, and mercury: strategies and challenges. Front Genet. 2014;5:201. doi: 10.3389/fgene.2014.00201
   PubMed Web of Science ®Google Scholar
• Kvist J, Gonçalves Athanàsio C, Shams Solari O, et al. Pattern of DNA methylation in Daphnia: evolutionary perspective. Genome Biol Evol. 2018;10(8):1988–2007. doi: 10.1093/gbe/evy155
   PubMed Web of Science ®Google Scholar
• Thaulow J, Song Y, Lindeman LC, et al. Epigenetic, transcriptional and phenotypic responses in Daphnia magna exposed to low-level ionizing radiation. Environ Res. 2020;190:109930. doi: 10.1016/j.envres.2020.109930
   PubMed Web of Science ®Google Scholar
• ASTM, 1980. Standard practice for conducting acute toxicity tests with fishes, macroinvertebrates and amphibians. Report E 729-80, American Society for Testing and Materials, Philadelphia.
   Google Scholar
• Stein JR. Handbook of phycological methods-culture methods and growth measurements. Cambridge: Cambridge University Press; 1973.
   Google Scholar
• OECD. OECD guideline for testing of chemicals 202 - Daphnia sp., acute immobilisation test. Paris: OECD Publishing; 2004.
   Google Scholar
• Chomczynski P, Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987;162(1):156–159. doi: 10.1016/0003-2697(87)90021-2
   PubMed Web of Science ®Google Scholar
• Ozáez I, Aquilino M, Morcillo G, et al. UV filters induce transcriptional changes of different hormonal receptors in chironomus riparius embryos and larvae. Environ Pollut. 2016;214:239–247. doi: 10.1016/j.envpol.2016.04.023
   PubMed Web of Science ®Google Scholar
• Poynton HC, Varshavsky JR, Chang B, et al. Daphnia magna ecotoxicogenomics provides mechanistic insights into metal toxicity. Environ Sci Technol. 2007;41(3):1044–1050. doi: 10.1021/es0615573
   PubMed Web of Science ®Google Scholar
• Pfaffl MW. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 2001;29(9):45e–45. doi: 10.1093/nar/29.9.e45
   PubMed Web of Science ®Google Scholar
• Asselman J, Glaholt SP, Smith Z, et al. Functional characterization of four metallothionein genes in Daphnia pulex exposed to environmental stressors. Aquat Toxicol. 2012;110–111:54–65. doi: 10.1016/j.aquatox.2011.12.010
   PubMed Web of Science ®Google Scholar
• De Coninck DIM, Asselman J, Glaholt S, et al. Genome-wide transcription profiles reveal genotype-dependent responses of biological pathways and gene-families in daphnia exposed to single and mixed stressors. Environ Sci Technol. 2014;48:3513–3522. doi: 10.1021/es4053363
   PubMed Web of Science ®Google Scholar
• Vandegehuchte MB, Lemière F, Vanhaecke L, et al. Direct and transgenerational impact on daphnia magna of chemicals with a known effect on DNA methylation. Comp Biochem Physiol - C Toxicol Pharmacol. 2010b;151(3):278–285. doi: 10.1016/j.cbpc.2009.11.007
   PubMed Web of Science ®Google Scholar
• Barata C, Varo I, Navarro JC, et al. Antioxidant enzyme activities and lipid peroxidation in the freshwater cladoceran daphnia magna exposed to redox cycling compounds. Comp Biochem Physiol - C Toxicol Pharmacol. 2005;140(2):175–186. doi: 10.1016/j.cca.2005.01.013
   PubMed Web of Science ®Google Scholar
• Pellegri V, Gorbi G, Buschini A. DNA damage detection by comet assay on daphnia magna: application in freshwater biomonitoring. Sci Total Environ. 2020;705:135780. doi: 10.1016/j.scitotenv.2019.135780
   PubMed Web of Science ®Google Scholar
• Suresh S, Crease TJ, Cristescu ME, et al. Alternative splicing is highly variable among daphnia pulex lineages in response to acute copper exposure. BMC Genomics. 2020;21(1):433. doi: 10.1186/s12864-020-06831-4
   PubMed Web of Science ®Google Scholar
• Asselman J, Shaw JR, Glaholt SP, et al. Transcription patterns of genes encoding four metallothionein homologs in Daphnia pulex exposed to copper and cadmium are time- and homolog-dependent. Aquat Toxicol. 2013;142–143:422–430. doi: 10.1016/j.aquatox.2013.09.010
   PubMed Web of Science ®Google Scholar
• Sekelsky J. DNA repair in drosophila: mutagens, models, and missing genes. Genetics. 2017;205(2):471–490. doi: 10.1534/genetics.116.186759
   PubMed Web of Science ®Google Scholar
• Song Y, Rundberget JT, Evenseth LM, et al. Whole-organism transcriptomic analysis provides mechanistic insight into the acute toxicity of emamectin benzoate in daphnia magna. Environ Sci Technol. 2016;50(21):11994–12003. doi: 10.1021/acs.est.6b03456
   PubMed Web of Science ®Google Scholar
• Song Y, Xie L, Lee YK, et al. Integrative assessment of low-dose gamma radiation effects on daphnia magna reproduction: toxicity pathway assembly and AOP development. Sci Total Environ. 2020;705:135912. doi: 10.1016/j.scitotenv.2019.135912
   PubMed Web of Science ®Google Scholar
• Tang S, Wu Y, Ryan CN, et al. Distinct expression profiles of stress defense and DNA repair genes in Daphnia pulex exposed to cadmium, zinc, and quantum dots. Chemosphere. 2015;120:92–99. doi: 10.1016/j.chemosphere.2014.06.011
   PubMed Web of Science ®Google Scholar
• Decaestecker E, Labbé P, Ellegaard K, et al. Candidate innate immune system gene expression in the ecological model Daphnia. Dev Comp Immunol. 2011;35(10):1068–1077. doi: 10.1016/j.dci.2011.04.004
   PubMed Web of Science ®Google Scholar
• Nash N, Klymasz-Swartz AK, Nash MT, et al. Impact of heatwaves and environmental ammonia on energy metabolism, nitrogen excretion, and mRNA expression of related genes in the indicator model system daphnia magna. Aquat Toxicol. 2022;249:106225. doi: 10.1016/j.aquatox.2022.106225
   PubMed Web of Science ®Google Scholar
• Pilorz V, Helfrich-Förster C, Oster H. The role of the circadian clock system in physiology. Pflugers Arch Eur J Physiol. 2018;470(2):227–239. doi: 10.1007/s00424-017-2103-y
   PubMed Web of Science ®Google Scholar
• Tilden AR, McCoole MD, Harmon SM, et al. Genomic identification of a putative circadian system in the cladoceran crustacean daphnia pulex. Comp Biochem Physiol. 2011;6(3):282–309. doi: 10.1016/j.cbd.2011.06.002
   Google Scholar
• Cai M, Liu Z, Yu P, et al. Circadian rhythm regulation of the oxidation–antioxidant balance in Daphnia pulex. Comp Biochem Physiol Part - B Biochem Mol Biol. 2020;240:110387. doi: 10.1016/j.cbpb.2019.110387
   PubMed Web of Science ®Google Scholar
• Coldsnow KD, Relyea RA, Hurley JM. Evolution to environmental contamination ablates the circadian clock of an aquatic sentinel species. Ecol Evol. 2017;7(23):10339–10349. doi: 10.1002/ece3.3490
   PubMed Web of Science ®Google Scholar
• Asselman J, De Coninck DI, Beert E, et al. Bisulfite sequencing with daphnia highlights a role for epigenetics in regulating stress response to microcystis through preferential differential methylation of serine and threonine amino acids. Environ Sci Technol. 2017;51(2):924–931. doi: 10.1021/acs.est.6b03870
   PubMed Web of Science ®Google Scholar
• Schermelleh L, Haemmer A, Spada F, et al. Dynamics of Dnmt1 interaction with the replication machinery and its role in postreplicative maintenance of DNA methylation. Nucleic Acids Res. 2007;35(13):4301–4312. doi: 10.1093/nar/gkm432
   PubMed Web of Science ®Google Scholar
• Foulkes WD, Priest JR, Duchaine TF. DICER1: mutations, microRNAs and mechanisms. Nat Rev Cancer. 2014;14(10):662–672. doi: 10.1038/nrc3802
   PubMed Web of Science ®Google Scholar
• Coucheron DH, Wojewodzic MW, Bøhn T. MicroRNAs in Daphnia magna identified and characterized by deep sequencing, genome mapping and manual curation. Sci Rep. 2019;9(1):1–15. doi: 10.1038/s41598-019-52387-z
   PubMedGoogle Scholar
• Hearn J, Chow FWN, Barton H, et al. Daphnia magna microRnas respond to nutritional stress and ageing but are not transgenerational. Mol Ecol. 2018;27(6):1402–1412. doi: 10.1111/mec.14525
   PubMed Web of Science ®Google Scholar
• Poreba E, Lesniewicz K, Durzynska J. Histone–lysine N-methyltransferase 2 (KMT2) complexes – a new perspective. Mutat Res. 2022;790:108443. doi: 10.1016/j.mrrev.2022.108443
   Google Scholar
• Yang X. The diverse superfamily of lysine acetyltransferases and their roles in leukemia and other diseases. Nucleic Acids Res. 2004;32(3):959–976. doi: 10.1093/nar/gkh252
   PubMed Web of Science ®Google Scholar
• Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 2011;21(3):381–395. doi: 10.1038/cr.2011.22
   PubMed Web of Science ®Google Scholar
• Lawrence M, Daujat S, Schneider R. Lateral thinking: how histone modifications regulate gene expression. Trends Genet. 2016;32(1):42–56. doi: 10.1016/j.tig.2015.10.007
   PubMed Web of Science ®Google Scholar
• Dai H, Wang Z. Histone modification patterns and their responses to environment. Curr Environ Heal Reports. 2014;1(1):11–21. doi: 10.1007/s40572-013-0008-2
   Google Scholar
• Suarez-Ulloa V, Gonzalez-Romero R, Eirin-Lopez JM. Environmental epigenetics: a promising venue for developing next-generation pollution biomonitoring tools in marine invertebrates. Mar Pollut Bull. 2015;98(1–2):5–13. doi: 10.1016/j.marpolbul.2015.06.020
   PubMed Web of Science ®Google Scholar
• Bossuyt BTA, Janssen CR. Influence of multigeneration acclimation to copper on tolerance, energy reserves, and homeostasis of Daphnia magna Straus. Environ Toxicol Chem. 2004;23(8):2029–2037. doi: 10.1897/03-377
   PubMed Web of Science ®Google Scholar
• Bossuyt BTA, Janssen CR. Acclimation of Daphnia magna to environmentally realistic copper concentrations. Comp Biochem Physiol - C Toxicol Pharmacol. 2003;136(3):253–264. doi: 10.1016/j.cca.2003.09.007
   PubMed Web of Science ®Google Scholar
• Engelen E, Janssens RC, Yagita K, et al. Mammalian TIMELESS is Involved in period determination and DNA damage-dependent phase advancing of the circadian clock. PLoS One. 2013;8(2):e56623. doi: 10.1371/journal.pone.0056623
   PubMed Web of Science ®Google Scholar
• Masri S, Kinouchi K, Sassone-Corsi P. Circadian clocks, epigenetics, and cancer. Curr Opin Oncol. 2015;27(1):50–56. doi: 10.1097/CCO.0000000000000153
   PubMed Web of Science ®Google Scholar
• Sahar S, Sassone-Corsi P. The epigenetic language of circadian clocks. In: Kramer A Merrow M, editors. Circadian clocks. Springer; 2013. pp. 29–44. doi: 10.1007/978-3-642-25950-0_2.
   Google Scholar
• Leung JM, Martinez ME. Circadian rhythms in Environmental Health Sciences. Curr Environ Heal Reports. 2020;7(3):272–281. doi: 10.1007/s40572-020-00285-2
   PubMedGoogle Scholar