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Effects of Copper on Calcium Metabolism and Detoxification Mechanisms in Freshwater Bivalve Species of Anodonta

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Effects of Copper on Calcium Metabolism and Detoxification Mechanisms in Freshwater Bivalve Species of Anodonta University of Bayreuth, Germany Chair of Environmental Chemistry and Ecotoxicology & University of Lorraine, France Laboratory of Interactions Ecotoxicology Biodiversity Ecosystems Thesis submitted in fulfillment of the degree of Doctor in Sciences Discipline: Ecotoxicology Effects of copper on calcium metabolism and detoxification mechanisms in freshwater bivalve species of Anodonta Olivier SANTINI 13 June 2012 Supervisors: Professor Hartmut FRANK Professor Paule VASSEUR University of Bayreuth, Germany Chair of Environmental Chemistry and Ecotoxicology & University of Lorraine, France Laboratory of Interactions Ecotoxicology Biodiversity Ecosystems Thesis submitted in fulfillment of the degree of Doctor in Sciences Discipline: Ecotoxicology Effects of copper on calcium metabolism and detoxification mechanisms in freshwater bivalve species of Anodonta Olivier SANTINI 13 June 2012 Supervisors: Professor Hartmut FRANK Professor Paule VASSEUR Jury of thesis: Lecturer-HDR Carole COSSU-LEGUILLE, University of Lorraine, France Professor Konrad DETTNER, University of Bayreuth, Germany, reviewer Professor Hartmut FRANK, University of Bayreuth, Germany, reviewer Professor Britta PLANER-FRIEDRICH, University of Bayreuth, Germany, chairman Professor Jouni TASKINEN University of Jyväskylä, Finland, reviewer Professor Paule VASSEUR University of Lorraine, France, reviewer This doctoral thesis was prepared at the Departement of Environmental Chemistry and Ecotoxicology in the University of Bayreuth supervised by Prof. Dr. Hartmut Frank, and in the Laboratory Interactions Ecotoxicology Biodiversity Ecosystems in the University of Lorraine supervised by Prof. Dr. Paule Vasseur, from 01/10/2006 until 13/06/2012. This is a full reprint of the dissertation submitted to attain the academic degree of the Doctor of Natural Sciences (Dr. rer. nat.) and approved by the Faculty of Biology, Chemistry and Geosciences of the University of Bayreuth. Acting Dean: Prof. Dr. Beate Lohnert Date of submission: 11/01/2012 Date of defence (disputation): 13/06/2012 Doctoral Committee: Lecturer-HDR Carole Cossu-Leguille Prof. Dr. Konrad Dettner Reviewer Prof. Dr. Hartmut Frank Reviewer Prof. Dr. Britta Planer-Friedrich Chairman Prof. Dr. Jouni Taskinen Reviewer Prof. Dr. Paule Vasseur Reviewer Acknowledgements I am very grateful to Professor Konrad Dettner, Professor Britta Planer-Friedrich, and Professor Jouni Taskinen, to participate in the jury of defense of this Ph.D, and to accept reviewing this Ph.D. thesis. I thank Professor Pascale Bauda, Professor Laure Giambérini, and Professor Jean François Ferard, the present and past directors of the laboratory, for welcoming me into the Laboratory Interactions Ecotoxicology Biodiversity Ecosystems (LIEBE). I wish to express my sincere gratitude to my two Supervisors, Professor Hartmut Frank and Professor Paule Vasseur who welcomed me in their teams. I am indebted to my supervisors for their guidance, for all of their valuable advices and remarks throughout this Ph.D. thesis. I thank Doctor Naima Chahbane, Lecturer-HDR Carole Cossu-Leguille, and Doctor Silke Gerstmann for their interest in this research and their help. My warm thanks to Mrs Agnes Bednorz for her kindness and her help. I am indebted to Lecturer Sylvie Cotelle for allowing me to use the HPLC equipment. I acknowledge Mr Philippe Rousselle for copper determinations by GFAAS and FAAS. Many thanks to Mrs Catherine Drui, Mrs Maryline Goergen and Mrs Irmgard Lauterbach, for their help in administrative issues. I am pleased to acknowledge all the colleagues for their kindness and their cheerfulness: Karen Burga, Anna Maria Becker, Cédric Mondy, Hugues Clivot, Audrey Cordi, Anne- Sophie Foltete, Eric Gismondi, Nelly Jacquet, Stéphane Jomini, Huong Thi Thuy Ngo, Nubia Quiroz, Guillermo Restrepo, Benjamin Schmidt, Didier Techer, Rosy Toda, Hela Toumi, Philippe Wagner, Monika Weckert, and sorry for those I may have forgotten in the above lines. 1 Thanks to my parents and my family for their constant support and their trust in me. And of course thank you, Céline, for all you give me every day, which allowed me to hold on and makes me happy. 2 Table of contents Acknowledgements .................................................................................................................... 1 List of publications or manuscripts and author’s contribution ................................................... 5 List of abbreviations ................................................................................................................... 6 List of figures ............................................................................................................................. 9 List of tables ............................................................................................................................. 11 Summary .................................................................................................................................. 12 Zusammenfassung .................................................................................................................... 13 Résumé ..................................................................................................................................... 14 1 General introduction .............................................................................................................. 32 2 Background ........................................................................................................................... 35 2.1 Copper ............................................................................................................................ 35 2.1.1 Origin and use ......................................................................................................... 35 2.1.2 Sources of emissions and environmental levels ...................................................... 37 2.1.3 Copper metabolism and its physiological role in animals (generalities)................. 40 2.1.4 Toxicology of copper (general) ............................................................................... 42 2.2 Biological models studied: Anodonta anatina and Anodonta cygnea ............................ 44 2.2.1 Taxonomy, description, and distribution ................................................................. 44 2.2.2 Anatomy and ecology .............................................................................................. 48 2.2.3 Ecotoxicological interest ......................................................................................... 50 2.3 Effects of copper exposure and detoxification mechanisms .......................................... 51 2.3.1 Copper exposure effects .......................................................................................... 51 2.3.1.1 Copper bioaccumulation .................................................................................. 51 2.3.1.2 Oxidative stress ................................................................................................ 53 2.3.1.3 Calcium transport and perturbation of bio-mineralization ............................... 55 2.3.2 Detoxification mechanisms ..................................................................................... 58 2.3.2.1 Cysteine thiol rich compounds ......................................................................... 58 2.3.2.2 Metal detoxification mechanisms in bivalves .................................................. 62 3 Extended summary ................................................................................................................ 67 3.1 Optimization of analytical protocols .............................................................................. 67 3.2 Effects of copper on calcium transport in Anodonta anatina ......................................... 71 3.3 Metal detoxification mechanism in Anodonta cygnea ................................................... 75 3.4 Decline of the Unionidae populations ............................................................................ 78 4 Conclusion ............................................................................................................................. 80 5 Article 1 (published): Effects of low-level copper exposure on Ca2+-ATPase and carbonic anhydrase in the freshwater bivalve Anodonta anatina ........................................................... 82 6 Article 2: Copper effects on Na+/K+-ATPase and H+-ATPase in the freshwater bivalve Anodonta anatina ..................................................................................................................... 94 3 7 Article 3: Phytochelatins in the freshwater bivalve Anodonta cygnea ................................ 108 8 Article 4: Phytochelatins, a group of metal-binding peptides induced by copper exposure in the bivalve Anodonta cygnea ................................................................................................. 121 References .............................................................................................................................. 135 Annexe ................................................................................................................................... 151 Ehrenwörtliche Erklärung ...................................................................................................... 155 4 List of publications or manuscripts and author’s contribution This Ph.D. dissertation is presented in cumulative form. It comprises
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