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University of Birmingham the Toxicogenome of Hyalella University of Birmingham The Toxicogenome of Hyalella azteca Poynton, Helen C.; Colbourne, John K.; Hasenbein, Simone; Benoit, Joshua B.; Sepulveda, Maria S.; Poelchau, Monica F.; Hughes, Daniel S.T.; Murali, Shwetha C.; Chen, Shuai; Glastad, Karl M.; Goodisman, Michael A.D.; Werren, John H.; Vineis, Joseph H.; Bowen, Jennifer L.; Friedrich, Markus; Jones, Jeffery; Robertson, Hugh M.; Feyereisen, René; Mechler-Hickson, Alexandra; Mathers, Nicholas DOI: 10.1021/acs.est.8b00837 License: None: All rights reserved Document Version Peer reviewed version Citation for published version (Harvard): Poynton, HC, Colbourne, JK, Hasenbein, S, Benoit, JB, Sepulveda, MS, Poelchau, MF, Hughes, DST, Murali, SC, Chen, S, Glastad, KM, Goodisman, MAD, Werren, JH, Vineis, JH, Bowen, JL, Friedrich, M, Jones, J, Robertson, HM, Feyereisen, R, Mechler-Hickson, A, Mathers, N, Lee, CE, Biales, A, Johnston, JS, Wellborn, GA, Rosendale, AJ, Cridge, AG, Munoz-Torres, MC, Bain, PA, Manny, AR, Major, KM, Lambert, FN, Vulpe, CD, Tuck, P, Blalock, BJ, Lin, YY, Smith, ME, Ochoa-Acuña, H, Chen, MJM, Childers, CP, Qu, J, Dugan, S, Lee, SL, Chao, H, Dinh, H, Han, Y, Doddapaneni, H, Worley, KC, Muzny, DM, Gibbs, RA & Richards, S 2018, 'The Toxicogenome of Hyalella azteca: A Model for Sediment Ecotoxicology and Evolutionary Toxicology', Environmental Science and Technology, vol. 52, no. 10, pp. 6009-6022. https://doi.org/10.1021/acs.est.8b00837 Link to publication on Research at Birmingham portal Publisher Rights Statement: This document is the Accepted Manuscript version of a Published Work that appeared in final form in Environmental Science and Technology, copyright © American Chemical Society after peer review and technical editing by the publisher. To access the final edited and published work see DOI: 10.1021/acs.est.8b00837. For non-commercial use only. General rights Unless a licence is specified above, all rights (including copyright and moral rights) in this document are retained by the authors and/or the copyright holders. The express permission of the copyright holder must be obtained for any use of this material other than for purposes permitted by law. •Users may freely distribute the URL that is used to identify this publication. •Users may download and/or print one copy of the publication from the University of Birmingham research portal for the purpose of private study or non-commercial research. •User may use extracts from the document in line with the concept of ‘fair dealing’ under the Copyright, Designs and Patents Act 1988 (?) •Users may not further distribute the material nor use it for the purposes of commercial gain. Where a licence is displayed above, please note the terms and conditions of the licence govern your use of this document. When citing, please reference the published version. Take down policy While the University of Birmingham exercises care and attention in making items available there are rare occasions when an item has been uploaded in error or has been deemed to be commercially or otherwise sensitive. If you believe that this is the case for this document, please contact [email protected] providing details and we will remove access to the work immediately and investigate. Download date: 23. Sep. 2021 1 The Toxicogenome of Hyalella azteca: a model for sediment ecotoxicology and 2 evolutionary toxicology 3 Helen C. Poynton1,*, Simone Hasenbein2, Joshua B. Benoit3, Maria S. Sepulveda4, Monica F. 4 Poelchau5, Daniel S.T. Hughes6, Swetha C. Murali6, Shuai Chen4,7, Karl M. Glastad8,9, Michael 5 A. D. Goodisman9, John H. Werren10, Joseph H. Vineis11, Jennifer L. Bowen11, Markus 6 Friedrich12, Jeffery Jones12, Hugh M. Robertson13, René Feyereisen14, Alexandra Mechler- 7 Hickson15, Nicholas Mathers15, Carol Eunmi Lee15, John K. Colbourne16, Adam Biales17, J. 8 Spencer Johnston18, Gary A. Wellborn19, Andrew J. Rosendale3, Andrew G. Cridge20, Monica C. 9 Munoz-Torres21, Peter A. Bain22, Austin R. Manny23, Kaley M. Major1, Faith Lambert24, Chris D. 10 Vulpe24, Padrig Tuck1, Bonnie Blalock1,Yu-Yu Lin25, , Mark E. Smith26, Hugo Ochoa-Acuña4, 11 Mei-ju May Chen25, Christopher P. Childers5, Jiaxin Qu6, Shannon Dugan6, Sandra L. Lee6, Hsu 12 Chao6, Huyen Dinh6, Yi Han6, HarshaVardhan Doddapaneni6, Kim C. Worley6, 27, Donna M. 13 Muzny6, Richard A. Gibbs6, Stephen Richards6 14 15 Affiliations 16 1. School for the Environment, University of Massachusetts Boston, Boston, MA 02125 United 17 States 18 2. Aquatic Systems Biology Unit, Technical University of Munich, D-85354 Freising, Germany 19 3. Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221 United 20 States 21 4. Forestry and Natural Resources, Purdue University, West Lafayette, IN 47907 United States 22 5. Agricultural Research Service, National Agricultural Library, USDA, Beltsville, MD 20705 23 United States 24 6. Human Genome Sequencing Center, Baylor College of Medicine, Houston, TX 77030 United 25 States 26 7. OmicSoft Corporation, Cary, NC 27513 United States 27 8. Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA 19104 United 28 States 29 9. School of Biological Sciences, Georgia Institute of Technology, Atlanta, GA 30332 United 30 States 31 10. Biology Department, University of Rochester, Rochester, NY 14627 United States 32 11. Department of Marine and Environmental Sciences, Marine Science Center, Northeastern 33 University, Nahant, MA 01908 United States 34 12. Wayne State University, Detroit MI 48202 United States 35 13. Department of Entomology, University of Illinois at Urbana-Champaign, Urbana, IL 61801 36 United States 37 14. Department of Plant and Environmental Sciences, University of Copenhagen, DK-1871 38 Frederiksberg, Denmark 39 15. Center of Rapid Evolution (CORE) and Department of Integrative Biology, University of 40 Wisconsin, Madison WI 53706 USA 41 16. School of Biosciences, University of Birmingham, Birmingham, B15 2TT UK 42 17. National Exposure Research Laboratory, United States Environmental Protection Agency, 43 Cincinnati, OH 45268 United States 44 18. Department of Entomology, Texas A&M University, College Station, TX 77843 USA 45 19. Department of Biology, University of Oklahoma, Norman, OK 73019 United States 1 46 20. Laboratory for Evolution and Development, Department of Biochemistry, University of 47 Otago, Dunedin, 9054 New Zealand 48 21. Environmental Genomics and Systems Biology Division, Lawrence Berkeley National 49 Laboratory, Berkeley, CA 94720 United States 50 22. Commonwealth Scientific and Industrial Research Organisation (CSIRO), Urrbrae SA, 5064 51 Australia 52 23. Department of Microbiology & Cell Science, University of Florida, Gainesville, FL 32611 53 United States 54 24. Center for Environmental and Human Toxicology, University of Florida, Gainesville, FL 55 32611 United States 56 25. Graduate Institute of Biomedical Electronics and Bioinformatics, National Taiwan University, 57 Taipei, 10617 Taiwan 58 26. McConnell Group, Cincinnati, OH 45268, United States 59 27. Department of Molecular and Human Genetics, Baylor College of Medicine, Houston, TX 60 77030 United States 61 62 *Corresponding author: Helen Poynton 63 School for the Environment, University of Massachusetts Boston 64 100 Morrissey Blvd., Boston, MA 02125, USA 65 [email protected] 66 67 68 Abstract 69 70 Hyalella azteca is a cryptic species complex of epibenthic amphipods of interest to 71 ecotoxicology and evolutionary biology. It is the primary crustacean used in North America for 72 sediment toxicity testing and an emerging model for molecular ecotoxicology. To provide 73 molecular resources for sediment quality assessments and evolutionary studies, we sequenced, 74 assembled, and annotated the genome of the H. azteca US Lab Strain. The genome quality 75 and completeness is comparable with other ecotoxicological model species. Through targeted 76 investigation and use of gene expression data sets of H. azteca exposed to pesticides, metals, 77 and other emerging contaminants, we annotated and characterized the major gene families 78 involved in sequestration, detoxification, oxidative stress, and toxicant response. Our results 79 revealed gene loss related to light sensing, but a large expansion in chemoreceptors, likely 80 underlying sensory shifts necessary in their low light habitats. Gene family expansions were 81 also noted for cytochrome P450 genes, cuticle proteins, ion transporters, and include recent 82 gene duplications in the metal sequestration protein, metallothionein. Mapping of differentially- 83 expressed transcripts to the genome significantly increased the ability to functionally annotate 84 toxicant responsive genes. The H. azteca genome will greatly facilitate development of 85 genomic tools for environmental assessments and promote an understanding of how evolution 86 shapes toxicological pathways with implications for environmental and human health. 2 87 TOC art: 88 89 90 91 3 92 Introduction 93 94 Sediment quality assessments serve as a metric for overall habitat integrity of freshwater 95 ecosystems. Sediments provide a foundation for aquatic food webs, providing habitat for 96 invertebrate species including crustaceans and insect larvae. However, they also concentrate 97 pollution over time, especially hydrophobic contaminants that sorb to sediments, leading to 98 bioaccumulation in the food web.1 While concentrations of a few legacy contaminants are 99 declining in the United States due to regulatory efforts;2 chemicals designed as their 100 replacements are becoming emerging
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