HAL Id: tel-03014095 https://tel.archives-ouvertes.fr/tel-03014095 Submitted on

HAL Id: tel-03014095 https://tel.archives-ouvertes.fr/tel-03014095 Submitted on 19 Nov 2020 HAL is a multi-disciplinary open access archive for the deposit and dissemination of sci- entific research documents, whether they are pub- lished or not. The documents may come from teaching and research institutions in France or abroad, or from public or private research centers. L’archive ouverte pluridisciplinaire HAL, est destinée au dépôt et à la diffusion de documents scientifiques de niveau recherche, publiés ou non, émanant des établissements d’enseignement et de recherche français ou étrangers, des laboratoires publics ou privés. Parental selenium and antioxidant status in fish. Pauline Wischhusen To cite this version: Pauline Wischhusen. Parental selenium and antioxidant status in fish.. Zootechny. Université de Pau et des Pays de l’Adour, 2020. English. ￿NNT : 2020PAUU3011￿. ￿tel-03014095￿ THÈSE UNIVERSITE DE PAU ET DES PAYS DE L’ADOUR ÉCOLE DOCTORALE 211 – SCIENCES EXACTES ET LEURS APPLICATIONS Présentée et soutenue le 18 Septembre 2020 par Pauline Paloma Cornelia WISCHHUSEN pour obtenir le grade de docteur de l’Université de Pau et des Pays de l’Adour Spécialité : Physiologie & Biologie des Organismes – Populations - Interactions Parental selenium and antioxidant status in fish *** Rôle du sélénium sur les fonctions anti-oxydantes des poissons géniteurs MEMBRES DU JURY RAPPORTEURS • Marisol IZQUIERDO Professeur / Université de Las Palmas de Gran Canaria (ES) • Brett GLENCROSS Professeur / Université de Stirling (UK) EXAMINATEURS • David MAZURAIS Chargé de Recherche / IFREMER • Brice BOUYSSIERE Professeur / Université de Pau et des Pays de l’Adour DIRECTEURS • Benoit FAUCONNEAU Directeur de Recherches / INRAE • Stéphanie FONTAGNÉ-DICHARRY Chargée de Recherche / INRAE Parental selenium and antioxidant status in fish Acknowledgement - 2 - Acknowledgement There are many who helped me along the way to complete this PhD and I want to take a moment to thank them. First, I would like to thank E2S: Energy and Environmental Solutions at the University of Pau amd Pays de l’Adour for letting me be part of the network and giving me the financial support to perform this PhD project at the National Research Institute for Agriculture, Food and the Environment in Saint-Pée-sur-Nivelle, France, including a six-month international mobility at the Institute of Marine Research in Bergen, Norway. I also want to thank Adisseo Company (especially Pierre-André Geraert and Mickael Briens) for financially supporting some part of the selenium feeding trial and sharing their interest in my research. Further, I would like to express my gratitude to the rapporteurs and examiners of the PhD jury: Brice Bouyssiere, Marisol Izquierdo, Brett Glencross and David Mazurais for generously offering their time, ideas and guidance through the dissertation process. I’m also thankful to my PhD supervisor Benoit Fauconneau for his thoughtful comments and recommendations. A special thank goes to my PhD co-supervisor Stéphanie Fontagné-Dicharry for her consistent support including all the conversations and meetings, for asking me intelligent questions or giving me such answers and gently pushing me to go a few extra steps throughout different parts of my PhD. It has been a pleasure working with you! I am also very grateful to my “hidden” supervisor, Philip Antony Jesu Prabhu, who was not at all staying in the background, but in contrary shared his knowledge, wisdom and motivation on selenium research in fish with me at any time, when I needed it or only just wanted to exchange ideas. In that regard, I also would like to acknowledge the support from all the members of the IMR laboratory in Norway. To name just a few: Kaja Skjӕrven, Kristin Hamre, Takaya Saito, Anne-Catrin Adam and Chandrasekar Selvam. I’m also grateful to Sachi Kaushik for doing “shadow guidance” in this project, helping me with advice in the background and introducing me to so many interesting people at the scientific conferences. I am thankful for the stimulating cooperations with the members of the IPREM laboratory in Pau, Sandra Mounicou, Maité Bueno and Carine Arnaudguilhem, who made me literally “see” my research topic and the members of the IBBM laboratory in Montpellier for insights in the isoprostanoid metabolism. I am also thankful to all the members of the INRAE lab, in St-Pee, at the fish farms and other places, who are too many to name here, but truly deserve my gratitude for their support and companionship during this time of PhD. Thanks to Laurence Larroquet, Cécile Heraud, Vincent Véron and Anne Surget for exellent analytical training and support. I am also very grateful for a range of other colleagues and friends, especially Jingwei, Luis, Maroussia, Simon, Hengtong, Guillaume, Thérèse, Lokesh, Felix, Claudia, Melissa, “Dephi’s Gang!” and Maike. In the end, a word to my family: Ohne Eure Unterstützung hätte ich es nicht hierher geschafft, und ich bin froh, euch an meiner Seite zu haben - Vielen Dank! Parental selenium and antioxidant status in fish TABLE OF CONTENTS - 3 - TABLE OF CONTENTS 1. GENERAL INTRODUCTION ...................................................................................................................................... 8 1.1. Fish to feed the world ........................................................................................................................................ 9 1.2. Fishmeal and fish oil reduction for more sustainability .................................................................. 10 1.3. Impact on micronutrient levels .................................................................................................................. 11 1.4. Risk of selenium deficiency .......................................................................................................................... 12 2. LITERATURE REVIEW ............................................................................................................................................ 14 2.1. Antioxidant system, the basics [24]........................................................................................................... 15 2.2. Discovery of selenium as essential micronutrient ............................................................................. 16 2.3. The selenium cycle ........................................................................................................................................... 16 2.3.1. Selenium in the environment.............................................................................................................. 16 2.3.2. Environmental contamination by selenium ................................................................................. 18 2.4. Selenium in plants ............................................................................................................................................ 19 2.4.1. Uptake ........................................................................................................................................................... 19 2.4.2. Metabolism in plants .............................................................................................................................. 20 2.5. Metabolism in humans and animals ......................................................................................................... 21 2.6. Selenium in proteins ....................................................................................................................................... 23 2.7. Selenoproteins ................................................................................................................................................... 23 2.7.1. Synthesis ...................................................................................................................................................... 23 2.7.2. Hierarchical regulation .......................................................................................................................... 24 2.7.3. Sexual dimorphism ................................................................................................................................. 25 2.8. Selenoproteome ................................................................................................................................................ 26 2.8.1. Mammalian selenoproteome .............................................................................................................. 26 2.8.2. Specificities of the fish selenoproteome ......................................................................................... 39 2.9. Selenium, seleno-compounds and the antioxidant system ............................................................. 42 2.10. Selenium and reproduction ....................................................................................................................... 43 Parental selenium and antioxidant status in fish TABLE OF CONTENTS - 4 - 2.11. The concept of nutritional programming ............................................................................................ 45 2.12. Selenium and epigenetics ........................................................................................................................... 47 2.13. Selenium in human nutrition and health ............................................................................................. 49 2.14. Selenium supplementation in terrestrial agriculture ..................................................................... 50 2.14.1. Supplementation form ........................................................................................................................ 50 2.14.2. Selenium in poultry production ...................................................................................................... 51 2.14.3. Selenium in mammalian farm animals ......................................................................................... 51 2.15. Selenium in fish nutrition ........................................................................................................................... 52 3. OBJECTIVES OF THE PHD...................................................................................................................................... 56 3.1. Reproductive performance and parental selenium transfer (Paper 1) ..................................... 57 3.2. Selenium imaging in the progeny (Paper 2) ......................................................................................... 57 3.3. Long-term parental effects on fry performance and stress resistance after first feeding (Paper 3) ....................................................................................................................................................................... 58 3.4. Interactions between selenium and the one-carbon metabolism (Paper 4 and Paper 5) . 58 4. MATERIAL AND METHODS .................................................................................................................................. 59 4.1. Experimental diets ........................................................................................................................................... 60 4.2. Experimental design ....................................................................................................................................... 62 4.3. Sampling............................................................................................................................................................... 63 4.4. Sample analysis ................................................................................................................................................. 64 5. PUBLICATIONS .......................................................................................................................................................... 65 5.1. Publication 1 ....................................................................................................................................................... 67 5.2. Publication 2 ....................................................................................................................................................... 81 5.3. Publication 3 ..................................................................................................................................................... 109 5.4. Publication 4 ..................................................................................................................................................... 125 5.5. Publication 5 ..................................................................................................................................................... 150 6. GENERAL DISCUSSION ......................................................................................................................................... 180 6.1. Dietary selenium supplementation in non-supplemented fishmeal-free diet reveals sub- optimal levels at different developmental stages ..................................................................................... 181 Parental selenium and antioxidant status in fish TABLE OF CONTENTS - 5 - 6.2. Selenium analysis revealed differences in tissue Se localization and Se composition pending on dietary selenium form .................................................................................................................. 184 6.3. Parental selenium improved the antioxidant status of the offspring in short-term but long-term studies gave unexpected changes in the metabolism of glutathione........................... 186 6.4. Selenium interferes in the one-carbon metabolism and causes changes in DNA methylation pattern of genes that reveal new potential target pathways of parental selenium ........................................................................................................................................................................................ 188 6.5. Complex interaction between parental nutritional history, direct selenium nutrition, selenium form and other environmental stimuli ...................................................................................... 190 7. CONCLUSION AND PERSPECTIVES ................................................................................................................. 192 7.1. Conclusion ......................................................................................................................................................... 193 7.2. Perspectives ...................................................................................................................................................... 194 8. REFERENCES ............................................................................................................................................................ 196 ANNEX .............................................................................................................................................................................. 219 LIST OF PUBLICATIONS ............................................................................................................................................ 231 LIST OF COMMUNICATIONS ................................................................................................................................... 232 Parental selenium and antioxidant status in fish List of figures - 6 - List of figures Fig. 1. World fish utilization and apparent consumption. Source: FAO [1] .............................................. 9 Fig. 2. World Capture Fishery and Aquaculture production. Source: FAO [1] ..................................... 10 Fig. 3. Geographical representation of modeled soil Se content by Jones et al [30] ......................... 17 Fig. 4. Schematic selenium cycle. Source: Godin [34] ..................................................................................... 18 Fig. 5 Selenium metabolism in plants. Source: Terry et al [44] .................................................................. 20 Fig. 6. Metabolism of dietary selenocompounds. Source: Speckmann and Grune [21] .................... 21 Fig. 7. Metabolism of inorganic seleno-compounds by GSH and TrxR. Adapted from Lu et al. [54] ............................................................................................................................................................................................... 22 Fig. 8. SeCys biosynthesis pathway in mammalian cells (A) and structure of SECIS element (B). Adapted from Papp et al [17] ................................................................................................................................... 24 Fig. 9. Domain structure of SelP and its function. Source: Saito and Takahashi [89] ........................ 28 Fig. 10. Reaction sequence of TrxR-mediated reduction of protein disulfides. Source: Tinkov et al. [96]................................................................................................................................................................................. 29 Fig. 11. Catalytic cycle of glutathione peroxidases. Source: Brigelius-Flohé and Maiorino [98] .. 31 Fig. 12. Basic deiodinase reaction for the activation of T4 to T3. Modified from Bianco and Kim uploads/Litterature/ thesiswischhusen.pdf

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