Transcriptomic response and hydrocarbon accumulation in the eastern oyster (Crassostrea virginica) exposed to crude oil

Aguilar, 2012, American oyster (Crassostrea virginica) and sediments as a coastal zone pollution monitor by heavy metals, Int. J. Environ. Sci. Technol., 9, 579, 10.1007/s13762-012-0078-y Akcha, 2000, Enzymatic biomarker measurement and study of DNA adduct formation in benzo [a] pyrene-contaminated mussels, Mytilus galloprovincialis, Aquat. Toxicol., 49, 269, 10.1016/S0166-445X(99)00082-X Akira, 2006, Pathogen recognition and innate immunity, Cell, 124, 783, 10.1016/j.cell.2006.02.015 Amiard-Triquet, 2013, Introduction, 1 Amiard-Triquet, 2015, Individual biomarkers, 153 Anderson, 2015, Meta-analysis of studies using suppression subtractive hybridization and microarrays to investigate the effects of environmental stress on gene transcription in oysters, PLoS One, 10, 10.1371/journal.pone.0118839 Benjamini, 1995, Controlling the false discovery rate: a practical and powerful approach to multiple testing, J. R. Stat. Soc., 57, 289 Bhagavan, 2015 Biswas, 2013, Biological averaging in RNA-seq, arXiv preprint Blackburn, 2014 Blanchette, 2007, Marine glutathione S-transferases, Mar. Biotechnol., 9, 513, 10.1007/s10126-007-9034-0 Bolger, 2014, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics, 30, 2114, 10.1093/bioinformatics/btu170 Boutet, 2004, Response of the Pacific oyster Crassostrea gigas to hydrocarbon contamination under experimental conditions, Gene, 329, 147, 10.1016/j.gene.2003.12.027 Boutet, 2016, UniProtKB/Swiss-Prot, the manually annotated section of the UniProt KnowledgeBase: How to use the entry view, vol. 1374, 23 Brown-Peterson, 2015, A multiple endpoint analysis of the effects of chronic exposure to sediment contaminated with Deepwater Horizon oil on juvenile southern flounder and their associated microbiomes, Aquat. Toxicol., 165, 197, 10.1016/j.aquatox.2015.06.001 Bustamante, 2012, Bioaccumulation and metabolization of 14C-pyrene by the Pacific oyster Crassostrea gigas exposed via seawater, Chemosphere, 87, 938, 10.1016/j.chemosphere.2012.01.049 Caffrey, 2016, Living oysters and their shells as sites of nitrification and denitrification, Mar. Pollut. Bull., 112, 86, 10.1016/j.marpolbul.2016.08.038 Cai, 2014, Deep sequencing-based transcriptome profiling analysis of Chlamys farreri exposed to benzo [a] pyrene, Gene, 551, 261, 10.1016/j.gene.2014.09.003 Chapman, 2013, Assessing and managing sediment contamination in transitional waters, Environ. Int., 55, 71, 10.1016/j.envint.2013.02.009 Chen, 2001, MAP kinases, Chem. Rev., 101, 2449, 10.1021/cr000241p Cossu-Leguille, 2013, Aquatic biomarkers, 49 Cruz-Rodrıguez, 2002, Heat-shock protein (HSP70) response in the eastern oyster, Crassostrea virginica, exposed to PAHs sorbed to suspended artificial clay particles and to suspended field contaminated sediments, Aquat. Toxicol., 60, 157, 10.1016/S0166-445X(02)00008-5 Davies, 2012, Integrated marine environmental monitoring of chemicals and their effects, ICES Cooperative Research Report, 315 dos Reis, 2015, Histological responses and localization of the cytochrome P450 (CYP2AU1) in Crassostrea brasiliana exposed to phenanthrene, Aquat. Toxicol., 169, 79, 10.1016/j.aquatox.2015.10.011 Droege, 2008, The genome sequencer FLX system-longer reads, more applications, straight forward bioinformatics and more complete data sets, J. Biotechnol., 136, 3, 10.1016/j.jbiotec.2008.03.021 Eisler, 1987, Polycyclic aromatic hydrocarbon hazards to fish, wildlife, and invertebrates: a synoptic review, U.S. Fish and Wildlife Service Biological Report, 85, 1 Enwere, 2009 Epelboin, 2016, The Kinome of Pacific oyster Crassostrea gigas, its expression during development and in response to environmental factors, PLoS One, 11, 10.1371/journal.pone.0155435 Ertl, 2016, Combined exposure to pyrene and fluoranthene and their molecular effects on the Sydney rock oyster, Saccostrea glomerata, Aquat. Toxicol., 177, 136, 10.1016/j.aquatox.2016.05.012 Finch, 2016, Photo-enhanced toxicity of two weathered Macondo crude oils to early life stages of the eastern oyster (Crassostrea virginica), Mar. Pollut. Bull., 113, 316, 10.1016/j.marpolbul.2016.10.008 Fingas, 2001 Freire, 2003, The Prestige: impacts on resources and marine ecosystems, 104 Frouin, 2007, Physiological effects of polycyclic aromatic hydrocarbons on soft-shell clam Mya arenaria, Aquat. Toxicol., 82, 120, 10.1016/j.aquatox.2007.02.005 Garret, 2017 Gauthier, 2014, Metal–PAH mixtures in the aquatic environment: a review of co-toxic mechanisms leading to more-than-additive outcomes, Aquat. Toxicol., 154, 253, 10.1016/j.aquatox.2014.05.026 Ghiselli, 2012, De novo assembly of the Manila clam Ruditapes philippinarum transcriptome provides new insights into expression bias, mitochondrial doubly uniparental inheritance and sex determination, Molecular Biology Evolution, 29, 771, 10.1093/molbev/msr248 Glaser, 1981, Trace analyses for wastewaters, Environ. Sci. Technol., 15, 1426, 10.1021/es00094a002 Grabherr, 2011, Full-length transcriptome assembly from RNA-Seq data without a reference genome, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 Grundy, 1996, Immune inhibition in marine mussels by polycyclic aromatic hydrocarbons, Mar. Environ. Res., 42, 187, 10.1016/0141-1136(95)00033-X Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis, Nat. Protoc., 8, 1494, 10.1038/nprot.2013.084 Hampel, 2016, Biomarkers and effects Hu, 2016, LcGST4 is an anthocyanin-related glutathione S-transferase gene in Litchi chinensis Sonn, Plant Cell Rep., 35, 831, 10.1007/s00299-015-1924-4 Jenny, 2016, Transcriptomic evaluation of the American oyster, Crassostrea virginica, deployed during the Deepwater Horizon oil spill: evidence of an active hydrocarbon response pathway, Mar. Environ. Res., 120, 166, 10.1016/j.marenvres.2016.08.006 Jeong, 2007, Long-term effect of polycyclic aromatic hydrocarbon on physiological metabolisms of the Pacific oyster, Crassostrea gigas, Aquaculture, 265, 343, 10.1016/j.aquaculture.2007.02.021 Jiang, 2016, Transcriptomic responses of Perna viridis embryo to benzo(a)pyrene exposure elucidated by RNA sequencing, Chemosphere, 163, 125, 10.1016/j.chemosphere.2016.07.091 Jing-Jing, 2009, Effects of benzo [a] pyrene on DNA damage and histological alterations in gonad of scallop Chlamys farreri, Mar. Environ. Res., 67, 47, 10.1016/j.marenvres.2008.10.006 Jørgensen, 2005, Biotransformation of the polycyclic aromatic hydrocarbon pyrene in the marine polychaete Nereis virens, Environ. Toxicol. Chem., 24, 2796, 10.1897/05-047R.1 Karatolos, 2011, Pyrosequencing the transcriptome of the greenhouse whitefly, Trialeurodes vaporariorum reveals multiple transcripts encoding insecticide targets and detoxifying enzymes, BMC Genomics, 12, 56, 10.1186/1471-2164-12-56 Karnauskas, 2013, Ecosystem status report for the Gulf of Mexico, NOAA Technical Memorandum NMFS-SEFSC, 653, 52 Kendziorski, 2003, The efficiency of pooling mRNA in microarray experiments, Biostatistics, 4, 465, 10.1093/biostatistics/4.3.465 Kendziorski, 2005, On the utility ofpooling biological samples in microarray experiments, Proc. Natl. Acad. Sci., 102, 4252, 10.1073/pnas.0500607102 Kennedy, 2013, Xenobiotic protection/resistance mechanisms in organisms, 689 Kennish, M. J. 1991. Ecology of Estuaries: Anthropogenic Effects, vol. 1. CRC Press, Boca Raton, FL, USA. 494 pp. Kirby, 2019 Köhler, 2001, The hepatic stress protein (hsp70) response to interacting abiotic parameters in fish exposed to various levels of pollution, J. Aquat. Ecosyst. Stress. Recover., 8, 261, 10.1023/A:1012935931161 Lacroix, 2014, A selection of reference genes and early-warning mRNA biomarkers for environmental monitoring using Mytilus spp. as sentinel species, Mar. Pollut. Bull., 86, 304, 10.1016/j.marpolbul.2014.06.049 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 Lech, 1980, Relationship between biotransformation and the toxicity and fate of xenobiotic chemicals in fish, Environmental Health Perspective, 34, 115, 10.1289/ehp.8034115 Leung, 2014, De novo transcriptome analysis of Perna viridis highlights tissue-specific patterns for environmental studies, BMC Genomics, 15, 804, 10.1186/1471-2164-15-804 Li, 2011, RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome, BMC bioinformatics, 12, 323, 10.1186/1471-2105-12-323 Li, 2017, Characterization of transcriptome and identification of biomineralization genes in winged pearl oyster (Pteria penguin) mantle tissue, Comparative Biochemistry and Physiology Part D: Genomics and Proteomics, 21, 67 Livingstone, 1998, The fate of organic xenobiotics in aquatic ecosystems: quantitative and qualitative differences in biotransformation by invertebrates and fish, Comparative Biochemistry and Physiology - A Molecular and Integrative Physiology, 120, 43, 10.1016/S1095-6433(98)10008-9 Lopes, 2012, Responses of CYP450 dependent system to aliphatic and aromatic hydrocarbons body burden in transplanted mussels from South coast of Portugal, Ecotoxicology, 21, 730, 10.1007/s10646-011-0834-7 Lüchmann, 2012, Suppressive subtractive hybridization libraries prepared from the digestive gland of the oyster Crassostrea brasiliana exposed to a diesel fuel water-accommodated fraction, Environ. Toxicol. Chem., 31, 1249, 10.1002/etc.1837 Lüchmann, 2014, A light in the darkness: New biotransformation genes, antioxidant parameters and tissue-specific responses in oysters exposed to phenanthrene, Aquat. Toxicol., 152, 324, 10.1016/j.aquatox.2014.04.021 Martínez-Gómez, 2010, A guide to toxicity assessment and monitoring effects at lower levels of biological organization following marine oil spills in European waters, ICES J. Mar. Sci., 67, 1105, 10.1093/icesjms/fsq017 McDowell, 2014, Transcriptome of American oysters, Crassostrea virginica, in response to bacterial challenge: insights into potential mechanisms of disease resistance, PLoS One, 9, 10.1371/journal.pone.0105097 Meador, 2003, Bioaccumulation of PAH's in marine invertebrates, 147 Men, 2009, Distributions of polycyclic aromatic hydrocarbons in the Daliao River Estuary of Liaodong Bay, Bohai Sea (China), Mar. Pollut. Bull., 58, 818, 10.1016/j.marpolbul.2009.01.022 Miao, J., Pan, L., Liu, N., Xu, C., Zhang, L. 2011. Molecular cloning of CYP4 and GSTpi homologues in the scallop Chlamys farreri and its expression in response to benzo[a]pyrene exposure. Marine genomics,4(2), 99-108. Murphy Neff, J. M. 1979. Polycyclic Aromatic Hydrocarbons in the Aquatic Environment: Sources, Fates and Biological Effects. Applied Science, Barking, Essex, UK, 262 pp. Neff, 2002 Neff, 1985, Petroleum contamination and biochemical-alterations in oysters (Crassostrea gigas) and plaice (Pleuronectes platessa) from bays impacted by the Amoco-Cadiz crude-oil spill, Mar. Environ. Res., 17, 281, 10.1016/0141-1136(85)90106-0 Neff, 2000, Effects of weathering on the toxicity of three offshore Australian crude oils and a diesel fuel to marine animals, Environ. Toxicol. Chem., 19, 1809, 10.1002/etc.5620190715 Newell, 2005, Influence of eastern oysters on nitrogen and phosphorus regeneration in Chesapeake Bay, USA, vol. 47, 93 Nogueira, 2017, Effects of phenanthrene on early development of the Pacific oyster Crassostrea gigas (Thunberg, 1789), Aquat. Toxicol., 191, 50, 10.1016/j.aquatox.2017.07.022 Noh, 2015, Fisetin regulates TPA-induced breast cell invasion by suppressing matrix metalloproteinase-9 activation via the PKC/ROS/MAPK pathways, Eur. J. Pharmacol., 764, 79, 10.1016/j.ejphar.2015.06.038 Omar-Ali, 2015, Tissue PAH, blood cell and tissue changes following exposure to water accommodated fractions of crude oil in alligator gar, Atractosteus spatula, Mar. Environ. Res., 108, 33, 10.1016/j.marenvres.2015.04.011 Parcellier, 2003, Heat shock proteins, cellular chaperones that modulate mitochondrial cell death pathways, Biochem. Biophys. Res. Commun., 304, 505, 10.1016/S0006-291X(03)00623-5 Patnaik, 2016, Sequencing, de novo assembly, and annotation of the transcriptome of the endangered freshwater pearl bivalve, Cristaria plicata, provides novel insights into functional genes and marker discovery, PLoS One, 11, 10.1371/journal.pone.0148622 Petrulis, 2001, Application of the ethoxyresorufin-O-deethylase (EROD) assay to mixtures of halogenated aromatic compounds, Environ. Toxicol., 16, 177, 10.1002/tox.1022 Piazza, 2016, Exposure to phenanthrene and depuration: changes on gene transcription, enzymatic activity and lipid peroxidation in gill of scallops Nodipecten nodosus, Aquat. Toxicol., 177, 146, 10.1016/j.aquatox.2016.05.025 Prada-Ríos, 2006, Acute toxicity and bioaccumulation of two polycyclic aromatic hydrocarbons (naphthalene and fluoranthene) in a bivalve mollusc, Boletín Científico CCCP, 13, 53 Rajkumar, 2015, Experimental validation of methods for differential gene expression analysis and sample pooling in RNA-Seq, BMC Genomics, 16, 548, 10.1186/s12864-015-1767-y Rewitz, 2004, Identification of two Nereis virens (Annelida: Polychaeta) cytochromes P450 and induction by xenobiotics, Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 138, 89 Rewitz, 2006, Marine invertebrate cytochrome P450: emerging insights from vertebrate and insect analogies, Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 143, 363 Reynaud, 2006, The effects of polycyclic aromatic hydrocarbons on the immune system of fish: a review, Aquat. Toxicol., 77, 229, 10.1016/j.aquatox.2005.10.018 Riches, 2009, Quantitative evaluation of the expression and activity of five major sulfotransferases (SULTs) in human tissues: the SULT “pie”, Drug Metab. Dispos., 37, 2255, 10.1124/dmd.109.028399 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics, 26, 139, 10.1093/bioinformatics/btp616 Roméo, 2013, History of biomarkers, 15 Roméo, 2011, Biotransformation of organics contaminants and the acquisition of resistance, 175 SAGARPA, 2013 Sambrook, J., Maccallum, P., Russel, D. 2001. Molecular Cloning: A Laboratory Manual, Third ed. Cold Springs Harbour Press, NY, USA. 2222 pp. Schäfer, 2009, Gonadal lesions of female sea urchin (Psammechinus miliaris) after exposure to the polycyclic aromatic hydrocarbon phenanthrene, Mar. Environ. Res., 68, 128, 10.1016/j.marenvres.2009.05.001 Schuler, 2001, Sequence alignment and database searching, vol. 43, 187 Schurch, 2016, How many biological replicates are needed in an RNA-seq experiment and which differential expression tool should you use?, RNA, 22, 839, 10.1261/rna.053959.115 Sericano, 1996, Accumulation and depuration of organic contaminants by the American oyster (Crassostrea virginica), Sci. Total Environ., 179, 149, 10.1016/0048-9697(96)90054-6 Shumway, 1996, Natural environmental factors, 467 Sindermann, C. J. 2006. Coastal Pollution: Effects on Living Resources and Humans. CRC Press, Boca Raton, Florida, USA. 306 pp. Sistema de Venecia, 1958, Symposium on the classification of brackish waters, Venice April 8–14, 1958, Archives Oceanography and Limnology, 11, 1 Snyder, 2000, Cytochrome P450 enzymes in aquatic invertebrates: recent advances and future directions, Aquat. Toxicol., 48, 529, 10.1016/S0166-445X(00)00085-0 Srivastava, 2002, Roles of heat-shock proteins in innate and adaptive immunity, Nat. Rev. Immunol., 2, 185, 10.1038/nri749 Tian, 2013, An investigation of endocrine disrupting effects and toxic mechanisms modulated by benzo [a] pyrene in female scallop Chlamys farreri, Aquat. Toxicol., 144, 162, 10.1016/j.aquatox.2013.09.031 Tolosa, 2005, Aliphatic and aromatic hydrocarbons in marine biota and coastal sediments from the Gulf and the Gulf of Oman, Mar. Pollut. Bull., 50, 1619, 10.1016/j.marpolbul.2005.06.029 Tymoczko, J. L., Berg, J. M., Stryer, L. 2013. Biochemistry: A Short Course. Second edition. Macmillan Education, New York, NY, USA. 862 pp. Valavanidis, 2006, Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants, Ecotoxicol. Environ. Saf., 64, 178, 10.1016/j.ecoenv.2005.03.013 Van der Oost, 2003, Fish bioaccumulation and biomarkers in environmental risk assessment: a review, Environ. Toxicol. Pharmacol., 13, 57, 10.1016/S1382-6689(02)00126-6 Vargas, 2003, Stromal cell-derived receptor 2 and cytochrome b561 are functional ferric reductases, Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics, 1651, 116, 10.1016/S1570-9639(03)00242-5 Varney, 2009, Population genetics of the eastern oyster Crassostrea virginica (Gmelin, 1791) in the Gulf of Mexico, J. Shellfish Res., 28, 855, 10.2983/035.028.0415 Vignet, 2016, Fish reproduction is disrupted upon lifelong exposure to environmental PAHs fractions revealing different modes of action, Toxics, 4, 10.3390/toxics4040026 Wang, 2003, Kinetics study of endogenous heat shock protein 70 expression, J. Biomech. Eng., 125, 794, 10.1115/1.1632522 Wang, 2016, RNA-seq analysis revealed ROS-mediated related genes involved in cadmium detoxification in the razor clam Sinonovacula constricta, Fish & shellfish immunology, 57, 350, 10.1016/j.fsi.2016.08.051 Wang, 2018, The oyster immunity, Developmental & Comparative Immunology, 80, 99, 10.1016/j.dci.2017.05.025 Widdows, 1982, Responses of Mytilus edulis on exposure to the water-accommodated fraction of North Sea oil, Mar. Biol., 67, 15, 10.1007/BF00397090 Wrigth, D. A., Welburn, P. 2002. Environmental Toxicology, vol. 11. Cambridge University Press, New York, USA. 630 pp. Xu, 2012, RNA-Seq analysis implicates dysregulation of the immune system in schizophrenia, BMC Genomics, 13, S2, 10.1186/1471-2164-13-S8-S2 Yang, 2014, A new fibrinogen-related protein from Argopecten irradians (AiFREP-2) with broad recognition spectrum and bacteria agglutination activity, Fish & shellfish immunology, 38, 221, 10.1016/j.fsi.2014.03.025 Young, 2010, Gene ontology analysis for RNA-seq: accounting for selection bias, Genome Biol., 11, R14, 10.1186/gb-2010-11-2-r14 Zacchi, 2017, Transcriptional changes in oysters Crassostrea brasiliana exposed to phenanthrene at different salinities, Aquat. Toxicol., 183, 94, 10.1016/j.aquatox.2016.12.016 Zhang, 2012, Transcriptome analysis of the Octopus vulgaris central nervous system, BMC Genomics, 7 Zhang, 2012, The oyster genome reveals stress adaptation and complexity of shell formation, Nature, 490, 49, 10.1038/nature11413 Zhang, 2014, Transcriptome analysis reveals a rich gene set related to innate immunity in the eastern oyster (Crassostrea virginica), Mar. Biotechnol., 16, 17, 10.1007/s10126-013-9526-z