Metabolomic Investigations of the Temporal Effects of Exposure to Pharmaceuticals and Personal Care Products and Their Mixture in the Eastern Oyster (Crassostrea virginica).


Journal

Environmental toxicology and chemistry
ISSN: 1552-8618
Titre abrégé: Environ Toxicol Chem
Pays: United States
ID NLM: 8308958

Informations de publication

Date de publication:
02 2020
Historique:
received: 29 04 2019
revised: 21 05 2019
accepted: 22 10 2019
pubmed: 30 10 2019
medline: 18 8 2020
entrez: 30 10 2019
Statut: ppublish

Résumé

The eastern oyster (Crassostrea virginica) supports a large aquaculture industry and is a keystone species along the Atlantic seaboard. Native oysters are routinely exposed to a complex mixture of contaminants that increasingly includes pharmaceuticals and personal care products (PPCPs). Unfortunately, the biological effects of chemical mixtures on oysters are poorly understood. Untargeted gas chromatography-mass spectrometry metabolomics was utilized to quantify the response of oysters exposed to fluoxetine, N,N-diethyl-meta-toluamide, 17α-ethynylestradiol, diphenhydramine, and their mixture. Oysters were exposed to 1 µg/L of each chemical or mixture for 10 d, followed by an 8-d depuration period. Adductor muscle (n = 14/treatment) was sampled at days 0, 1, 5, 10, and 18. Trajectory analysis illustrated that metabolic effects and class separation of the treatments varied at each time point and that, overall, the oysters were only able to partially recover from these exposures post-depuration. Altered metabolites were associated with cellular energetics (i.e., Krebs cycle intermediates), as well as amino acid metabolism and fatty acids. Exposure to these PPCPs also affected metabolic pathways associated with anaerobic metabolism, osmotic stress, and oxidative stress, in addition to the physiological effects of each chemical's postulated mechanism of action. Following depuration, fewer metabolites were altered, but none of the treatments returned them to their initial control values, indicating that metabolic disruptions were long-lasting. Interestingly, the mixture did not directly cluster with individual treatments in the scores plot from partial least squares discriminant analysis, and many of its affected metabolic pathways were not well predicted from the individual treatments. The present study highlights the utility of untargeted metabolomics in developing exposure biomarkers for compounds with different modes of action in bivalves. Environ Toxicol Chem 2020;39:419-436. © 2019 SETAC.

Identifiants

pubmed: 31661721
doi: 10.1002/etc.4627
doi:

Substances chimiques

Cosmetics 0
Water Pollutants, Chemical 0
Fluoxetine 01K63SUP8D
DEET 134-62-3

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

419-436

Subventions

Organisme : Procter & Gamble Fellowship for Doctoral Research in Environmental Science
Pays : International

Informations de copyright

© 2019 SETAC.

Références

Adamo SA. 2008. Norepinephrine and octopamine: Linking stress and immune function across phyla. Invertebrate Surviv J 5:12-19.
Akberali HB, Trueman ER. 1985. Effects of environmental stress on marine bivalve molluscs. In Blaxter JHS, Russell FS, Yonge M, eds, Advances in Marine Biology, Vol 22. Academic, London, UK, pp 101-198.
Akutsu T, Kobayashi K, Sakurada K, Ikegaya H, Furihata T, Chiba K. 2007. Identification of human cytochrome p450 isozymes involved in diphenhydramine N-demethylation. Drug Metab Dispos 35:72-78.
Almeida Â, Calisto V, Esteves VI, Schneider RJ, Soares AM, Figueira E, Freitas R. 2018. Effects of single and combined exposure of pharmaceutical drugs (carbamazepine and cetirizine) and a metal (cadmium) on the biochemical responses of Ruditapes philippinarum. Aquat Toxicol 198:10-19.
Altenburger R, Scholz S, Schmitt-Jansen M, Busch W, Escher BI. 2012. Mixture toxicity revisited from a toxicogenomic perspective. Environ Sci Technol 46:2508-2522.
Ankley GT, Villeneuve DL. 2015. Temporal changes in biological responses and uncertainty in assessing risks of endocrine-disrupting chemicals: Insights from intensive time-course studies with fish. Toxicol Sci 144:259-275.
Ascenzi P, Bocedi A, Marino M. 2006. Structure-function relationship of estrogen receptor α and β: Impact on human health. Mol Aspects Med 27:299-402.
ASTM International. 2006. Standard guide for conducting laboratory toxicity tests with fresh-water mussels. E2455-06. In Annual Book of ASTM Standards, Vol 11.06. Philadelphia, PA, USA.
Backhaus T. 2014. Medicines, shaken and stirred: A critical review on the ecotoxicology of pharmaceutical mixtures. Philos Trans R Soc B Biol Sci 369:20130585.
Backhaus T, Porsbring T, Arrhenius Å, Brosche S, Johansson P, Blanck H. 2011. Single-substance and mixture toxicity of five pharmaceuticals and personal care products to marine periphyton communities. Environ Toxicol Chem 30:2030-2040.
Ballesta-Artero I, Witbaard R, Carroll ML, van der Meer J. 2017. Environmental factors regulating gaping activity of the bivalve Arctica islandica in northern Norway. Mar Biol 164:116.
Barber BJ, Blake NJ. 2006. Reproductive physiology. In Shumway SE, Parsons GJ, eds, Scallops: Biology, Ecology and Aquaculture, Vol 35-Developments in Aquaculture and Fisheries Science. Elsevier, Amsterdam, The Netherlands, pp 357-416.
Bartelt-Hunt SL, Snow DD, Damon T, Shockley J, Hoagland K. 2009. The occurrence of illicit and therapeutic pharmaceuticals in wastewater effluent and surface waters in Nebraska. Environ Pollut 157:786-791.
Baylay AJ, Spurgeon DJ, Svendsen C, Griffin JL, Swain SC, Sturzenbaum SR, Jones OAH. 2012. A metabolomics based test of independent action and concentration addition using the earthworm Lumbricus rubellus. Ecotoxicology 21:1436-1447.
Benotti MJ, Brownawell BJ. 2007. Distributions of pharmaceuticals in an urban estuary during both dry- and wet-weather conditions. Environ Sci Technol 41:5795-5802.
Berninger JP, Du B, Connors KA, Eytcheson SA, Kolkmeier MA, Prosser KN, Valenti TW Jr, Chambliss CK, Brooks BW. 2011. Effects of the antihistamine diphenhydramine on selected aquatic organisms. Environ Toxicol Chem 30:2065-2072.
Boxall A, Rudd MA, Brooks BW, Caldwell DJ, Choi K, Hickmann S, Innes E, Ostapyk K, Staveley JP, Verslycke T, Ankley GT, Beazley KF, Belanger SE, Berninger JP, Carriquiriborde P, Coors A, Deleo PC, Dyer SD, Ericson JF, Gagne F, Giesy JP, Gouin T, Hallstrom L, Karlsson MV, Larsson DG, Lazorchak JM, Mastrocco F, McLaughlin A, McMaster ME, Meyerhoff RD, Moore R, Parrott JL, Snape JR, Murray-Smith R, Servos MR, Sibley PK, Straub JO, Szabo ND, Topp E, Tetreault GR, Trudeau VL, Van, der Kraak G. 2012. Pharmaceuticals and personal care products in the environment: What are the big questions? Environ Health Perspect 120:1221-1229.
Bradley PM, Journey CA, Romanok KM, Barber LB, Buxton HT, Foreman WT, Furlong ET, Glassmeyer ST, Hladik ML, Iwanowicz LR, Jones DK, Kolpin DW, Kuivila KM, Loftin KA, Mills MA, Meyer MT, Orlando JL, Reilly TJ, Smalling KL, Villeneuve DL. 2017. Expanded target-chemical analysis reveals extensive mixed-organic-contaminant exposure in US streams. Environ Sci Technol 51:4792-4802.
Brausch JM, Connors KA, Brooks BW, Rand GM. 2012. Human pharmaceuticals in the aquatic environment: A review of recent toxicological studies and considerations for toxicity testing. Rev Environ Contam Toxicol 218:1-99.
Brown C, Corcoran E, Herkenrath P, Thonell J. 2006. Marine and coastal ecosystems and human well-being: Synthesis. United Nations Environment Programme, Nairobi, Kenya.
Brown NJ, Roberts LJ. 2001. Histamine, bradykinin, and their antagonists. In Hardman JG, Limbird LE, eds, Goodman and Gilman's The Pharmacological Basis of Therapeutics, 10th ed. McGraw-Hill, New York, NY, USA, pp 645-667.
Brunengraber H, Roe CR. 2006. Anaplerotic molecules: Current and future. J Inherit Metab Dis 29:327-331.
Bundy JG, Davey MP, Viant MR. 2009. Environmental metabolomics: A critical review and future perspectives. Metabolomics 5:3.
Burg MB, Ferraris JD. 2008. Intracellular organic osmolytes: Function and regulation. J Biol Chem 283:7309-7313.
Cailleaud K, Forget-Leray J, Peluhet L, LeMenach K, Souissi S, Budzinski H. 2009. Tidal influence on the distribution of hydrophobic organic contaminants in the Seine estuary and biomarker responses on the copepod Eurytemora affinis. Environ Pollut 157:64-71.
Canesi L, Ciacci C, Betti M, Lorusso LC, Marchi B, Burattini S, Falcieri E, Gallo G. 2004. Rapid effects of 17β-estradiol on cell signaling and function of Mytilus hemocytes. Gen Comp Endocrinol 136:58-71.
Cappello T, Fernandes D, Maisano M, Casano A, Bonastre M, Bebianno MJ, Mauceri A, Fasulo S, Porte C. 2017. Sex steroids and metabolic responses in mussels Mytilus galloprovincialis exposed to drospirenone. Ecotoxicol Environ Saf 143:166-172.
Chan K, Truong D, Shangari N, O'Brien PJ. 2005. Drug-induced mitochondrial toxicity. Expert Opin Drug Metab Toxicol 1:655-669.
Chen H, Zha J, Yuan L, Wang Z. 2015. Effects of fluoxetine on behavior, antioxidant enzyme systems, and multixenobiotic resistance in the Asian clam Corbicula fluminea. Chemosphere 119:856-862.
Chinopoulos C. 2013. Which way does the citric acid cycle turn during hypoxia? The critical role of α-ketoglutarate dehydrogenase complex. J Neurosci Res 91:1030-1043.
Ciocan CM, Cubero-Leon E, Minier C, Rotchell JM. 2011. Identification of reproduction-specific genes associated with maturation and estrogen exposure in a marine bivalve Mytilus edulis. PLoS One 6:e22326.
Ciocan CM, Cubero-Leon E, Puinean AM, Hill EM, Minier C, Osada M, Fenlon K, Rotchell JM. 2010. Effects of estrogen exposure in mussels, Mytilus edulis, at different stages of gametogenesis. Environ Pollut 158:2977-2984.
Curtis TM, Williamson R, Depledge MH. 2000. Simultaneous, long-term monitoring of valve and cardiac activity in the blue mussel Mytilus edulis exposed to copper. Mar Biol 136:837-846.
Daughton CG, Brooks BW. 2011. Active pharmaceutical ingredients and aquatic organisms. In Beyer N, Meador J, eds, Environmental Contaminants in Biota: Interpreting Tissue Concentrations, 2nd ed. Taylor and Francis, Philadelphia, PA, USA, pp 287-347.
Debboun M, Frances SP, Strickman D. 2014. Insect Repellents Handbook. CRC, Boca Raton, FL, USA.
Denkert C, Budczies J, Weichert W, Wohlgemuth G, Scholz M, Kind T, Niesporek S, Noske A, Buckendahl A, Dietel M, Fiehn O. 2008. Metabolite profiling of human colon carcinoma-Deregulation of TCA cycle and amino acid turnover. Mol Cancer 7:72.
De Zwaan A, Wijsman TCM. 1976. Anaerobic metabolism in bivalvia (Mollusca). Characteristics of anaerobic metabolism. Comp Biochem Physiol B 54:313-323.
Di Poi C, Costil K, Bouchart V, Halm-Lemeille MP. 2018. Toxicity assessment of five emerging pollutants, alone and in binary or ternary mixtures, towards three aquatic organisms. Environ Sci Pollut Res 25:6122-6134.
Djordjevic J, Djordjevic A, Adzic M, Elaković I, Matić G, Radojcic MB. 2011. Fluoxetine affects antioxidant system and promotes apoptotic signaling in Wistar rat liver. Eur J Pharmacol 659:61-66.
Dsikowitzky L, Dwiyitno, Heruwati E, Ariyani F, Irianto HE, Schwarzbauer J. 2014. Exceptionally high concentrations of the insect repellent N,N-diethyl-m-toluamide (DEET) in surface waters from Jakarta, Indonesia. Environ Chem Lett 12:407-411.
Ebele AJ, Abou-Elwafa Abdallah M, Harrad S. 2017. Pharmaceuticals and personal care products (PPCPs) in the freshwater aquatic environment. Emerg Contam 3:1-16.
Ekman DR, Teng Q, Villeneuve DL, Kahl MD, Jensen KM, Durhan EJ, Ankley GT, Collette TW. 2008. Investigating compensation and recovery of fathead minnow (Pimephales promelas) exposed to 17α-ethynylestradiol with metabolite profiling. Environ Sci Technol 42:4188-4194.
Englert B. 2007. Method 1694: Pharmaceuticals and personal care products in water, soil, sediment, and biosolids by HPLC/MS/MS. US Environmental Protection Agency, Washington, DC.
Escher BI, Bramaz N, Eggen RI, Richter M. 2005. In vitro assessment of modes of toxic action of pharmaceuticals in aquatic life. Environ Sci Technol 39:3090-3100.
Fabbri E, Franzellitti S. 2015. Human pharmaceuticals in the marine environment: Focus on exposure and biological effects in animal species. Environ Toxicol Chem 35:799-812.
Fasulo S, Iacono F, Cappello T, Corsaro C, Maisano M, D'Agata A, Giannetto A, De Domenico E, Parrino V, Lo Paro G, Mauceri A. 2012. Metabolomic investigation of Mytilus galloprovincialis (Lamarck 1819) caged in aquatic environments. Ecotoxicol Environ Saf 84:139-146.
Fent K, Weston AA, Caminada D. 2006. Ecotoxicology of human pharmaceuticals. Aquat Toxicol 76:122-159.
Fernandes D, Pujol S, Aceña J, Perez S, Barceló D, Porte C. 2014. The in vitro interference of synthetic progestogens with carp steroidogenic enzymes. Aquat Toxicol 155:314-321.
Fernández C, Carbonell G, Babín M. 2013. Effects of individual and a mixture of personal-care products on cytotoxicity, EROD activity and ROS production in a rainbow trout gonadal cell line (RTG-2). J Appl Toxicol 33:1203-1212.
Fiehn O. 2002. Metabolomics-The link between genotypes and phenotypes. In Town D, ed, Functional genomics. Springer, Dordrecht, The Netherlands, pp 155-171.
Fong PP. 1998. Zebra mussel spawning is induced in low concentrations of putative serotonin reuptake inhibitors. Biol Bull 194:143-149.
Foreman RA III, Ellington WR. 1983. Effects of inhibitors and substrate supplementation on anaerobic energy metabolism in the ventricle of the oyster, Crassostrea virginica. Comp Biochem Physiol B Comp Biochem 74:543-547.
Franzellitti S, Buratti S, Capolupo M, Du B, Haddad SP, Chambliss CK, Brooks BW, Fabbri E. 2014. An exploratory investigation of various modes of action and potential adverse outcomes of fluoxetine in marine mussels. Aquat Toxicol 151:14-26.
Fuller SL. 2012. Effectiveness of oyster spat stick communities in removing pharmaceutical contaminants from tidal creeks. Masters thesis, University of Georgia, Athens, GA, USA. p 81.
Gabbott PA. 1976. Energy metabolism. In Bayne BL, ed, Marine Mussels: Their Ecology and Physiology. Cambridge University Press, Cambridge, UK, pp 293-356.
Gałecki P, Szemraj J, Biećkiewicz M, Florkowski A, Gałecka E. 2009. Lipid peroxidation and antioxidant protection in patients during acute depressive episodes and in remission after fluoxetine treatment. Pharmacol Rep 61:436-447.
Gamaro GD, Streck EL, Matté C, Prediger ME, Wyse AT, Dalmaz C. 2003. Reduction of hippocampal Na+,K+-ATPase activity in rats subjected to an experimental model of depression. Neurochem Res 28:1339-1344.
Gaw S, Thomas KV, Hutchinson TH. 2014. Sources, impacts and trends of pharmaceuticals in the marine and coastal environment. Philos Trans R Soc Lond B Biol Sci 369:20130572.
Gerhardt CC, Bakker RA, Piek GJ, Planta RJ, Vreugdenhil E, Leysen JE, Van Heerikhuizen H. 1997. Molecular cloning and pharmacological characterization of a molluscan octopamine receptor. Mol Pharmacol 51:293-300.
Gilroy ÈA, Klinck JS, Campbell SD, McInnis R, Gillis PL, de Solla SR. 2014. Toxicity and bioconcentration of the pharmaceuticals moxifloxacin, rosuvastatin, and drospirenone to the unionid mussel Lampsilis siliquoidea. Sci Total Environ 487:537-544.
Gonzalez-Rey M, Bebianno MJ. 2013. Does selective serotonin reuptake inhibitor (SSRI) fluoxetine affects mussel Mytilus galloprovincialis? Environ Pollut 173:200-209.
Granek EF, Conn KE, Nilsen EB, Pillsbury L, Strecker AL, Rumrill SS, Fish W. 2016. Spatial and temporal variability of contaminants within estuarine sediments and native Olympia oysters: A contrast between a developed and an undeveloped estuary. Sci Total Environ 557-558:869-879.
Grimbert S, Fromenty B, Fisch C, Letteron P, Berson A, Durand-Schneider AM, Feldmann G, Pessayre D. 1993. Decreased mitochondrial oxidation of fatty acids in pregnant mice: Possible relevance to development of acute fatty liver of pregnancy. Hepatology 17:628-637.
Harrison J, LaFleur K, Mantone D, Boisette B, Harris A, Catapane EJ, Carroll MA. 2015. The presence of histamine and a histamine receptor in the bivalve mollusc, Crassostrea virginica. In Vivo (Brooklyn) 36:123-130.
Hazelton PD, Du B, Haddad SP, Fritts AK, Chambliss CK, Brooks BW, Bringolf RB. 2014. Chronic fluoxetine exposure alters movement and burrowing in adult freshwater mussels. Aquat Toxicol 151:27-35.
Hemeryck A, Belpaire FM. 2002. Selective serotonin reuptake inhibitors and cytochrome P-450 mediated drug-drug interactions: An update. Curr Drug Metab 3:13-37.
Henry TB, Black MC. 2008. Acute and chronic toxicity of fluoxetine (selective serotonin reuptake inhibitor) in western mosquitofish. Arch Environ Contam Toxicol 54:325-330.
Hochachka PW, Mustafa T. 1972. Invertebrate facultative anaerobiosis. Science 178:1056-1060.
Hochachka PW, Somero GN. 2002. Biochemical Adaptation: Mechanism and Process in Physiological Evolution. Oxford University Press, New York, NY, USA.
Holbrook DJ Jr. 1987. Effects of toxicants on nucleic acid and protein metabolism. In Hodgson E, Smart RC, eds, Introduction to Biochemical Toxicology. John Wiley & Sons, New York, NY, USA, pp 325-342.
Holwerda DA, De Zwaan A, Kluytmans JH, Zandee DI. 1985. Metabolic adaptations to environmental anoxia in the intertidal bivalve mollusc Mytilus edulis L. Netherlands Journal of Zoology 36:322-343.
Hosoi M, Kubota S, Toyohara M, Toyohara H, Hayashi I. 2003. Effect of salinity change on free amino acid content in Pacific oyster. Fish Sci 69:395-400.
Huang SSY, Benskin JP, Veldhoen N, Chandramouli B, Butler H, Helbing CC, Cosgrove JR. 2017. A multi-omic approach to elucidate low-dose effects of xenobiotics in zebrafish (Danio rerio) larvae. Aquat Toxicol 182:102-112.
Jackson JE. 2005. A User's Guide to Principal Components, Vol. 587. John Wiley & Sons, Hoboken, NJ, USA.
Jones OAH, Swain SC, Svendsen C, Griffin JL, Sturzenbaum SR, Spurgeon DJ. 2012. Potential new method of mixture effects testing using metabolomics and Caenorhabditis elegans. J Proteome Res 11:1446-1453.
Jordan J, Zare A, Jackson LJ, Habibi HR, Weljie AM. 2012. Environmental contaminant mixtures at ambient concentrations invoke a metabolic stress response in goldfish not predicted from exposure to individual compounds alone. J Proteome Res 11:1133-1143.
Juhel G, Bayen S, Goh C, Lee WK, Kelly BC. 2017. Use of a suite of biomarkers to assess the effects of carbamazepine, bisphenol A, atrazine, and their mixtures on green mussels, Perna viridis. Environ Toxicol Chem 36:429-441.
Keun HC, Ebbels TMD, Bollard ME, Beckonert O, Antti H, Holmes E, Lindon JC, Nicholson JK. 2004. Geometric trajectory analysis of metabolic responses to toxicity can define treatment specific profiles. Chem Res Toxicol 17:579-587.
Krumsiek J, Bartel J, Theis FJ. 2016. Computational approaches for systems metabolomics. Curr Opin Biotechnol 39:198-206.
Länge R, Hutchinson TH, Croudace CP, Siegmund F, Schweinfurth H, Hampe P, Panter GH, Sumpter JP. 2001. Effects of the synthetic estrogen 17α-ethinylestradiol on the life-cycle of the fathead minnow (Pimephales promelas). Environ Toxicol Chem 20:1216-1227.
Lannig G, Eilers S, Pörtner HO, Sokolova IM, Bock C. 2010. Impact of ocean acidification on energy metabolism of oyster, Crassostrea gigas-Changes in metabolic pathways and thermal response. Mar Drugs 8:2318-2339.
Leonard JA, Cope WG, Barnhart MC, Bringolf RB. 2014. Metabolomic, behavioral, and reproductive effects of the synthetic estrogen 17 α-ethinylestradiol on the unionid mussel Lampsilis fasciola. Aquat Toxicol 150:103-116.
Li Y, Couch L, Higuchi M, Fang JL, Guo L. 2012. Mitochondrial dysfunction induced by sertraline, an antidepressant agent. Toxicol Sci 127:582-591.
Liu X, Zhang L, You L, Yu J, Zhao J, Li L, Wang Q, Li F, Li C, Liu D, Wu H. 2011. Differential toxicological effects induced by mercury in gills from three pedigrees of Manila clam Ruditapes philippinarum by NMR-based metabolomics. Ecotoxicology 20:177-186.
Livingstone DR, Bayne BL. 1974. Pyruvate kinase from the mantle tissue of Mytilus edulis L. Comp Biochem Physiol B Comp Biochem 48:481-497.
Lommen A. 2009. MetAlign: Interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. Anal Chem 81:3079-3086.
Lynch MP. 1965. The effects of environmental salinity on free amino acids of Crassostrea virginica. Master's thesis, College of William and Mary, Williamsburg, VA, USA.
Mager WH, de Boer AH, Siderius MH, Voss H-P. 2000. Cellular responses to oxidative and osmotic stress. Cell Stress Chaperones 5:73.
Matozzo V, Gagné F, Marin MG, Ricciardi F, Blaise C. 2008. Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: A review. Environ Int 34:531-545.
McEneff G, Barron L, Kelleher B, Paull B, Quinn B. 2013. The determination of pharmaceutical residues in cooked and uncooked marine bivalves using pressurised liquid extraction, solid-phase extraction and liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem 405:9509-9521.
Meador JP, Yeh A, Young G, Gallagher EP. 2016. Contaminants of emerging concern in a large temperate estuary. Environ Pollut 213:254-267.
Meek ME, Boobis AR, Crofton KM, Heinemeyer G, Van Raaij M, Vickers C. 2011. Risk assessment of combined exposure to multiple chemicals: A WHO/IPCS framework. Regul Toxicol Pharmacol 60(2 Suppl. 1):S1-S14.
Moore J. 2001. An Introduction to the Invertebrates. Cambridge University Press, Cambridge, UK.
Moreira DS, Aquino SF, Afonso RJ, Santos EP, de Pádua VL. 2009. Occurrence of endocrine disrupting compounds in water sources of Belo Horizonte Metropolitan Area, Brazil. Environ Technol 30:1041-1049.
Müller M, Mentel M, van Hellemond JJ, Henze K, Woehle C, Gould SB, Yu R, van der Giezen M, Tielens AGM, Martin WF. 2012. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol Mol Biol Rev 76:444-495.
Nelson DL, Lehninger AL, Cox MM. 2008. Lehninger Principles of Biochemistry. New York: Macmillan.
Ngo HTT, Gerstmann S, Frank H. 2011. Subchronic effects of environment-like cadmium levels on the bivalve Anodonta anatina (Linnaeus 1758): II. Effects on energy reserves in relation to calcium metabolism. Toxicol Environ Chem 93:1802-1814.
Niu W, Knight E, Xia Q, McGarvey BD. 2014. Comparative evaluation of eight software programs for alignment of gas chromatography-mass spectrometry chromatograms in metabolomics experiments. J Chromatogr A 1374:199-206.
Patience RL, Thomas JD, Sterry PR. 1983. Production and release of carboxylic acids during oxic and anoxic metabolism by the pulmonate snail Biomphalaria glabrata (Say). Comp Biochem Physiol B Comp Biochem 76:253-262.
Peters JR, Granek EF. 2016. Long-term exposure to fluoxetine reduces growth and reproductive potential in the dominant rocky intertidal mussel, Mytilus californianus. Sci Total Environ 545:621-628.
Prichard E, Granek EF. 2016. Effects of pharmaceuticals and personal care products on marine organisms: From single-species studies to an ecosystem-based approach. Environ Sci Pollut Res 23:22365-22384.
Purmal C, Kucejova B, Sherry AD, Burgess SC, Malloy CR, Merritt ME. 2014. Propionate stimulates pyruvate oxidation in the presence of acetate. Am J Physiol Heart Circ Physiol 307:H1134-H1141.
Roméo M, Mourgaud Y, Geffard A, Gnassia-Barelli M, Amiard JC, Budzinski H. 2003. Multimarker approach in transplanted mussels for evaluating water quality in Charentes, France, coast areas exposed to different anthropogenic conditions. Environ Toxicol 18:295-305.
Rozman KK, Doull J. 2000. Dose and time as variables of toxicity. Toxicology 144:169-178.
Roznere I, Watters GT, Wolfe BA, Daly M. 2017. Effects of relocation on metabolic profiles of freshwater mussels: Metabolomics as a tool for improving conservation techniques. Aquat Conserv 27:919-926.
Santos LH, Araújo AN, Fachini A, Pena A, Delerue-Matos C, Montenegro MCBSM. 2010. Ecotoxicological aspects related to the presence of pharmaceuticals in the aquatic environment. J Hazard Mater 175:45-95.
Saro L, Lopes I, Martins N, Ribeiro R. 2012. Testing hypotheses on the resistance to metals by Daphnia longispina: Differential acclimation, endpoints association, and fitness costs. Environ Toxicol Chem 31:909-915.
Scaini G, Maggi DD, De-Nês BT, Gonçalves CL, Ferreira GK, Teodorak BP, Bez GD, Ferreira GC, Schuck PF, Quevedo J, Streck EL. 2011. Activity of mitochondrial respiratory chain is increased by chronic administration of antidepressants. Acta Neuropsychiatr 23:112-118.
Schlenk D, Lavado R, Loyo-Rosales JE, Jones W, Maryoung L, Riar N, Sedlak D. 2012. Reconstitution studies of pesticides and surfactants exploring the cause of estrogenic activity observed in surface waters of the San Francisco Bay Delta. Environ Sci Technol 46:9106-9111.
Sehgal N, Goswami SV. 2001. Biochemical changes in the liver of the Indian freshwater murrel, Channa punctatus (Bloch) during estradiol-induced vitellogenin synthesis. Fish Physiol Biochem 24:149-155.
Silva LJG, Martins MC, Pereira AMPT, Meisel LM, Gonzalez-Rey M, Bebianno MJ, Lino CM, Pena A. 2016. Uptake, accumulation and metabolization of the antidepressant fluoxetine by Mytilus galloprovincialis. Environ Pollut 213:432-437.
Skelton DM, Ekman DR, Martinovic-Weigelt D, Ankley GT, Villeneuve DL, Teng Q, Collette TW. 2014. Metabolomics for in situ environmental monitoring of surface waters impacted by contaminants from both point and nonpoint sources. Environ Sci Technol 48(4):2395-2403.
Slaninova A, Modra H, Hostovsky M, Sisperova E, Blahova J, Matejova I, Vicenova M, Faldyna M, Zelnickova L, Tichy F, Svobodova Z. 2014. Effects of subchronic exposure to N,N-diethyl-m-toluamide on selected biomarkers in common carp (Cyprinus carpio L.). Biomed Res Int 2014:828515.
Song Q, Chen H, Li Y, Zhou H, Han Q, Diao X. 2016. Toxicological effects of benzo(a)pyrene, DDT and their mixture on the green mussel Perna viridis revealed by proteomic and metabolomic approaches. Chemosphere 144:214-224.
Southam AD, Lange A, Hines A, Hill EM, Katsu Y, Iguchi T, Tyler CR, Viant MR. 2011. Metabolomics reveals target and off-target toxicities of a model organophosphate pesticide to roach (Rutilus rutilus): Implications for biomonitoring. Environ Sci Technol 45:3759-3767.
Spurgeon DJ, Jones OA, Dorne JLC, Svendsen C, Swain S, Stürzenbaum SR. 2010. Systems toxicology approaches for understanding the joint effects of environmental chemical mixtures. Sci Total Environ 408:3725-3734.
Swale DR, Sun B, Tong F, Bloomquist JR. 2014. Neurotoxicity and mode of action of N,N-diethyl-meta-toluamide (DEET). PLoS One 9:e103713.
Tang R, Ding C, Ma Y, Wang J, Zhang T, Wang X. 2017. Time-dependent responses of earthworms to soil contaminated with low levels of lead as detected using 1H NMR metabolomics. RSC Adv 7:34170-34181.
Thibaut R, Schnell S, Porte C. 2006. The interference of pharmaceuticals with endogenous and xenobiotic metabolizing enzymes in carp liver: An in-vitro study. Environ Sci Technol 40:5154-5160.
Thompson DC, Perera K, London R. 2000. Spontaneous hydrolysis of 4-trifluoromethylphenol to a quinone methide and subsequent protein alkylation. Chem Biol Interact 126:1-14.
Thornton JW, Need E, Crews D. 2003. Resurrecting the ancestral steroid receptor: Ancient origin of estrogen signaling. Science 301:1714-1717.
Tikunov AP, Johnson CB, Lee H, Stoskopf MK, Macdonald JM. 2010. Metabolomic investigations of American oysters using 1H-NMR spectroscopy. Mar Drugs 8:2578-2596.
Tran TKA, MacFarlane GR, Kong RYC, O'Connor WA, Yu RMK. 2016. Potential mechanisms underlying estrogen-induced expression of the molluscan estrogen receptor (ER) gene. Aquat Toxicol 179:82-94.
Trenholm RA, Vanderford BJ, Holady JC, Rexing DJ, Snyder SA. 2006. Broad range analysis of endocrine disruptors and pharmaceuticals using gas chromatography and liquid chromatography tandem mass spectrometry. Chemosphere 65:1990-1998.
Tuffnail W, Mills GA, Cary P, Greenwood R. 2009. An environmental 1H NMR metabolomic study of the exposure of the marine mussel Mytilus edulis to atrazine, lindane, hypoxia and starvation. Metabolomics 5:33-43.
Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M. 2006. Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178-189.
Valdés ME, Marino DJ, Wunderlin DA, Somoza GM, Ronco AE, Carriquiriborde P. 2015. Screening concentration of E1, E2 and EE2 in sewage effluents and surface waters of the “Pampas” region and the “Rio de la Plata” estuary (Argentina). Bull Environ Contam Toxicol 94:29-33.
Viant MR. 2007. Revealing the metabolome of animal tissues using 1H nuclear magnetic resonance spectroscopy. In Weckwerth W, ed, Metabolomics, Vol 358-Methods in Molecular Biology. Humana, Totowa, NJ, USA, pp 229-246.
Wang W, Wu Z, Dai Z, Yang Y, Wang J, Wu G. 2013. Glycine metabolism in animals and humans: Implications for nutrition and health. Amino Acids 45:463-477.
Webhofer C, Gormanns P, Tolstikov V, Zieglgänsberger W, Sillaber I, Holsboer F, Turck CW. 2011. Metabolite profiling of antidepressant drug action reveals novel drug targets beyond monoamine elevation. Transl Psychiatry 1:e58.
Wittmer IK, Bader H-P, Scheidegger R, Singer H, Lück A, Hanke I, Carlsson C, Stamm C. 2010. Significance of urban and agricultural land use for biocide and pesticide dynamics in surface waters. Water Res 44:2850-2862.
Wong DT, Perry KW, Bymaster FP. 2005. The discovery of fluoxetine hydrochloride (Prozac). Nat Rev Drug Discov 4:764-774.
Wong RY, Oxendine SE, Godwin J. 2013. Behavioral and neurogenomic transcriptome changes in wild-derived zebrafish with fluoxetine treatment. BMC Genomics 14:348.
Xie Z, Lu G, Hou K, Qin D, Yan Z, Chen W. 2016. Bioconcentration, metabolism and effects of diphenhydramine on behavioral and biochemical markers in crucian carp (Carassius auratus). Sci Total Environ 544:400-409.
Yancey PH. 2005. Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819-2830.
Yeh A, Marcinek DJ, Meador JP, Gallagher EP. 2017. Effect of contaminants of emerging concern on liver mitochondrial function in Chinook salmon. Aquat Toxicol 190:21-31.
Yu Y, Huang Q, Cui J, Zhang K, Tang C, Peng X. 2011. Determination of pharmaceuticals, steroid hormones, and endocrine-disrupting personal care products in sewage sludge by ultra-high-performance liquid chromatography-tandem mass spectrometry. Anal Bioanal Chem 399:891-902.

Auteurs

David W Brew (DW)

Department of Environmental Health Science, University of Georgia, Athens, Georgia, USA.

Marsha C Black (MC)

Department of Environmental Health Science, University of Georgia, Athens, Georgia, USA.

Marina Santos (M)

Department of Environmental Health Science, University of Georgia, Athens, Georgia, USA.

Jackson Rodgers (J)

Department of Environmental Health Science, University of Georgia, Athens, Georgia, USA.

W Matthew Henderson (WM)

National Exposure Research Laboratory, Office of Research and Development, US Environmental Protection Agency, Athens, Georgia.

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