Transcriptome-level effects of the model organic pollutant phenanthrene and its solvent acetone in three amphipod species

Zhanna Shatilina1,2, Polina Drozdova1,3,4, Daria Bedulina1,2, Lorena Rivarola-Duarte3,4, Stephan Schreiber5, Christian Otto6, Frank Jühling7,8, Silke Aulhorn9, Wibke Busch9, Yulia Lubyaga1,2, Elizaveta Kondrateva1,10, Tamara Pobezhimova10, Lena Jakob11, Magnus Lucassen11, Franz J. Sartoris11, Jörg Hackermüller5, Hans-Otto Pörtner11, Peter F. Stadler3,12,13,14,15,16,4, Till Luckenbach9, Maxim Timofeyev1,2
1Institute of Biology, Irkutsk State University, Lenin str. 3, RUS-664003 Irkutsk, Russia
2Baikal Research Centre, Lenin str. 21, RUS-664003 Irkutsk, Russia
3Bioinformatics Group, Department of Computer Science, Universität Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
4Interdisciplinary Center for Bioinformatics, Universität Leipzig, Härtelstraße 16-18, D-04107 Leipzig, Germany
5Young Investigator Group Bioinformatics & Transcriptomics, UFZ – Helmholtz Centre for Environmental Research, Permoserstraße 15, D-04318 Leipzig, Germany
6ecSeq Bioinformatics GmbH, Sternwartenstraße 29, D-04103 Leipzig, Germany
7Inserm U1110, Institut de Recherche sur les Maladies Virales et Hépatiques, 3 Rue Koeberlé, F-67000 Strasbourg, France
8Université de Strasbourg, 4 Rue Blaise Pascal, F-67000 Strasbourg, France
9Department of Bioanalytical Ecotoxicology, UFZ – Helmholtz Centre for Environmental Research, Permoserstraße 15, D-04318 Leipzig, Germany
10Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch, RAS, Lermontov str. 132, 664033 Irkutsk, Russia
11Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, D-27570 Bremerhaven, Germany
12Competence Center for Scalable Data Services and Solutions Dresden/Leipzig, Interdisciplinary Center for Bioinformatics, German Centre for Integrative Biodiversity Research (iDiv), Leipzig Research Center for Civilization Diseases, Universität Leipzig, Augustusplatz 12, D-04107 Leipzig, Germany
13Max Planck Institute for Mathematics in the Sciences, Inselstraße 22, D-04103 Leipzig, Germany
14Department of Theoretical Chemistry, University of Vienna, Währinger Straße 17, A-1090 Vienna, Austria
15Facultad de Ciencias, Universidad National de Colombia, Sede Bogotá, Ciudad Universitaria, COL-111321 Bogotá, D.C., Colombia
16Santa Fe Institute, 1399 Hyde Park Rd., NM87501 Santa Fe, USA

Tài liệu tham khảo

Abdel-Shafy, 2016, A review on polycyclic aromatic hydrocarbons: source, environmental impact, effect on human health and remediation. Egypt, J. Petrol. (Online)., 25, 107 Alexa, 2009, Gene set enrichment analysis with topGO, Bioconductor Improv., 27 American Public Health Association, American Water Works Association, Water Environment Federation, 1998, Toxicity test systems, materials, and procedures. In: Standard Methods for the Examination of Water and Wastewater, 20th ed. APHA, Washington DC Antczak, 2013, Molecular toxicity identification evaluation (mTIE) approach predicts chemical exposure in Daphnia magna, Environ. Sci. Technol., 47, 11747, 10.1021/es402819c Bansal, 2017, Review of the quantification techniques for polycyclic aromatic hydrocarbons (PAHs) in food products, Crit. Rev. Food Sci. Nutr., 57, 3297, 10.1080/10408398.2015.1116970 Biales, 2013, Linkage of genomic biomarkers to whole organism end points in a toxicity identification evaluation (TIE), Environ. Sci. Technol., 47, 1306, 10.1021/es304274a Buchfink, 2014, Fast and sensitive protein alignment using DIAMOND, Nat. Methods, 12, 59, 10.1038/nmeth.3176 Chen, 2017, FunctionAnnotator, a versatile and efficient web tool for non-model organism annotation, Sci. Rep., 7 Cowgill, 1991, The sensitivity of Ceriodaphnia dubia and Daphnia magna to seven chemicals utilizing the three brood test, Arch. Environ. Contam. Toxicol., 20, 211, 10.1007/BF01055906 Dam, 2008, Cytochrome P450 expression is moult stage specific and regulated by ecdysteroids and xenobiotics in the crab Carcinus maenas, Biochem. Biophys. Res. Commun., 377, 1135, 10.1016/j.bbrc.2008.10.125 David, 2012, Interference with xenobiotic metabolic activity by the commonly used vehicle solvents dimethylsulfoxide and methanol in zebrafish (Danio rerio) larvae but not Daphnia magna, Chemosphere., 88, 912, 10.1016/j.chemosphere.2012.03.018 Deng, 2017, Removal of phenanthrene in contaminated soil by combination of alfalfa, white-rot fungus, and earthworms, Environ. Sci. Pollut. Res. Int., 24, 7565, 10.1007/s11356-017-8466-y Drozdova, P., 2019. Scripts used for data analysis of the acetone/phenanthrene treatment (submitted to CBPD). https://github.com/drozdovapb/EveEcyGlaDE/tree/master/CBPD_phenanthrene_scripts. Last accessed 13 September, 2019. Drozdova, 2019, Comparison between transcriptomic responses to short-term stress exposures of a common Holarctic and endemic Lake Baikal amphipods, BMC Genomics, 20, 712, 10.1186/s12864-019-6024-3 Ewell, 1986, Simultaneous evaluation of the acute effects of chemicals on seven aquatic species, Environ. Toxicol. Chem., 5, 831, 10.1002/etc.5620050908 Ghosal, 2016, Current state of knowledge in microbial degradation of polycyclic aromatic hydrocarbons (PAHs): a review, Front. Microbiol., 7, 1369 Grabherr, 2011, Trinity: reconstructing a full-length transcriptome without a genome from RNA-Seq data, Nat. Biotechnol., 29, 644, 10.1038/nbt.1883 Green, 2013, The use of carrier solvents in regulatory aquatic toxicology testing: practical, statistical and regulatory considerations. Aquat. toxicol., 144, 242, 10.1016/j.aquatox.2013.10.004 Haap, 2008, Acute effects of diclofenac and DMSO to Daphnia magna: immobilisation and hsp70-induction, Chemosphere., 73, 353, 10.1016/j.chemosphere.2008.05.062 Haas, 2013, De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis, Nature protoc., 8, 1494, 10.1038/nprot.2013.084 Hallare, 2006, Comparative embryotoxicity and proteotoxicity of three carrier solvents to zebrafish (Danio rerio) embryos, Ecotoxicol. Environ. Saf., 63, 378, 10.1016/j.ecoenv.2005.07.006 Huang, 2018, Unsuitable use of DMSO for assessing behavioral endpoints in aquatic model species, Sci. Total Environ., 615, 107, 10.1016/j.scitotenv.2017.09.260 Hutchinson, 2006, Acute and chronic effects of carrier solvents in aquatic organisms: a critical review, Aquat. Toxicol., 76, 69, 10.1016/j.aquatox.2005.09.008 Jakob, 2016, Lake Baikal amphipods under climate change: thermal constraints and ecological consequences, Ecosphere., 7, 10.1002/ecs2.1308 Kozhova, 1998 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923 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 Love, 2014, Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2, Genome Biol., 15, 550, 10.1186/s13059-014-0550-8 Marinković, 2012, Gene expression patterns and life cycle responses of toxicant-exposed chironomids, Environ. Sci. Technol., 46, 12679, 10.1021/es3033617 Marquis, 2006, Solvent toxicity to amphibian embryos and larvae, Chemosphere., 63, 889, 10.1016/j.chemosphere.2005.07.063 Moore, 2009, Climate change and the world's “Sacred sea” - Lake Baikal, Siberia, BioScience., 59, 405, 10.1525/bio.2009.59.5.8 Nota, 2009, Transcriptomics reveals extensive inducible biotransformation in the soil-dwelling invertebrate Folsomia candida exposed to phenanthrene, BMC Genomics, 10, 236, 10.1186/1471-2164-10-236 Novais, 2015, Normal operating range (NOR) in Enchytraeus albidus –transcriptional responses to control conditions, Appl. Soil Ecol., 85, 1, 10.1016/j.apsoil.2014.08.005 Ok, 2013, Characteristics of PAHs, PCDD/Fs, PCBs and PBDEs in the sediment of Lake Baikal, Russia, Polycycl. Aromat. Compd., 33, 173, 10.1080/10406638.2013.764540 van Ommen Kloeke, 2012, Molecular and life-history effects of a natural toxin on herbivorous and non-target soil arthropods, Ecotoxicology., 21, 1084, 10.1007/s10646-012-0861-z Patro, 2017, Salmon provides fast and bias-aware quantification of transcript expression, Nat. Methods, 14, 417, 10.1038/nmeth.4197 Pavlichenko, 2015, Identification of a putatively multixenobiotic resistance related Abcb1 transporter in amphipod species endemic to the highly pristine Lake Baikal, Environ. Sci. Pollut. Res. Int., 22, 5453, 10.1007/s11356-014-3758-y Poley, 2018, High level efficacy of lufenuron against sea lice (Lepeophtheirus salmonis) linked to rapid impact on moulting processes, Int. J. Parasitol. Drugs Drug Resist., 8, 174, 10.1016/j.ijpddr.2018.02.007 Potemkina, 2018, Climatic factors as risks of recent ecological changes in the shallow zone of Lake Baikal, Russ. Geol. Geophys., 59, 556, 10.1016/j.rgg.2018.04.008 Protopopova, 2014, Contrasting cellular stress responses of Baikalian and Palearctic amphipods upon exposure to humic substances: environmental implications, Environ. Sci. Pollut. Res. Int., 21, 14124, 10.1007/s11356-014-3323-8 R Core Team, 2017. A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. Vienna, Austria https://www.r-project.org/ Rayburn, 1997, Developmental toxicity of three carrier solvents using embryos of the grass shrimp, Palaemonetes pugio, Arch. Environ. Contam. Toxicol., 33, 217, 10.1007/s002449900246 Reid, 2018, Gene expression profiles of the Southern house mosquito Culex quinquefasciatus during exposure to permethrin, Insect sci., 25, 439, 10.1111/1744-7917.12438 Ren, 2015, Toxic effects upon exposure to benzo[a]pyrene in juvenile white shrimp Litopenaeus vannamei, Environ. Toxicol. Pharmacol., 39, 194, 10.1016/j.etap.2014.08.006 Rengarajan, 2015, Exposure to polycyclic aromatic hydrocarbons with special focus on cancer, Asian Pac. J. Trop. Biomed., 5, 182, 10.1016/S2221-1691(15)30003-4 Robinson, 2010, edgeR: a Bioconductor package for differential expression analysis of digital gene expression data, Bioinformatics., 26, 139, 10.1093/bioinformatics/btp616 Roelofs, 2016, Mechanisms of phenanthrene toxicity in the soil invertebrate, Enchytraeus crypticus, Environmental toxicology and chemistry, 35, 2713, 10.1002/etc.3433 Ruber, 1983, Effects of temephos on the respiratory rate of the salt marsh amphipod, Gammarus mucronatus, Bull. Environ. Contam. Toxicol., 31, 148, 10.1007/BF01607885 Sanz-Lázaro, 2008, Toxicity studies of polynuclear aromatic hydrocarbons (PAHs) on European amphipods, Toxicol. Mech. Methods, 18, 323, 10.1080/15376510701380273 Selderslaghs, 2009, Development of a screening assay to identify teratogenic and embryotoxic chemicals using the zebrafish embryo, Reprod. Toxicol., 28, 308, 10.1016/j.reprotox.2009.05.004 Semenov, 2018, Revealing the factors affecting occurrence and distribution of polycyclic aromatic hydrocarbons in water and sediments of Lake Baikal and its tributaries, Chem. Ecol., 34, 925, 10.1080/02757540.2018.1520848 Takhteev, 2015, Checklist of the Amphipoda (Crustacea) from continental waters of Russia, with data on alien species, Arthropoda Sel., 24, 335 The Committee on Methods for Acute Toxicity Testing with Aquatic Organisms, National Environmental Research Center, 1975 Timofeyev, 2006, Antioxidant response to natural organic matter (NOM) exposure in three Baikalean amphipod species from contrasting habitats, Comp. Biochem. Physiol. B: Biochem. Mol. Biol., 145, 197, 10.1016/j.cbpb.2006.07.004 Timofeyev, 2001, Attitude to temperature factor of some endemic amphipods from Lake Baikal and Holarctic Gammarus lacustris Sars, 1863: a comparative experimental study, Arthropoda Sel., 10, 93 Timofeyev, 2007, Natural organic matter (NOM) has the potential to modify the multixenobiotic resistance (MXR) activity in freshwater amphipods Eulimnogammarus cyaneus and E, verrucosus. Comp. Biochem. Physiol. B, Biochem. Mol. Biol., 146, 496, 10.1016/j.cbpb.2006.11.017 U.S. EPA, 2010. Standardized Analytical Methods for Environmental Restoration Following Homeland Security Events, SAM 2010 (SAM 6.0). EPA, Washington, DC. Appendix A to 40 CFR Part 423. retrieved from: http://www.epa.gov/waterscience/methods/pollutants.htm. . UNESCO, 1996. Lake Baikal. Retrieved from: https://whc.unesco.org/en/list/754 . Vache, 2007, A potential genomic biomarker for the detection of polycyclic aromatic hydrocarbon pollutants: multidrug resistance gene 49 in Drosophila melanogaster, Environ. Toxicol. Chem., 26, 1418, 10.1897/06-552R.1 Walker, 2008 Weis, 2015, Some physiological responses of crustaceans to toxicants, 4, 477 Yakan, 2013, Bioaccumulation—depuration kinetics and effects of phenanthrene on Mediterranean mussel (Mytilus galloprovincialis), J. Environ. Sci. Health A Tox. Hazard. Subst. Environ. Eng., 48, 1037, 10.1080/10934529.2013.773799 Zhang, 2000, The influence of feeding, photoperiod and selected solvents on the reproductive strategies of the water flea, Daphnia magna, Environ. Pollut., 110, 425, 10.1016/S0269-7491(99)00324-3