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Universidad De Murcia UNIVERSIDAD DE MURCIA FACULTAD DE BIOLOGÍA New Insights Into the Skin and Its Mucus in Teleost Fish Nuevas Perspectivas en el Estudio de la Piel y el Moco de Peces Teleósteos D. Héctor Cordero Muñoz 2016 Preface The present dissertation is submitted as a requirement for the degree of Philosophiae Doctor (PhD) at the Faculty of Biology in the University of Murcia (Spain).The different studies compiled in this dissertation represent original research carried out over a period of four years, as part of two projects entitled: -“Mucosal immunity on Mediterranean farmed fish (gilthead seabream and Senegalese sole). New advances in probiotic-mucosa and pathogen-mucosa interactions” (grant number AGL2011-30381-C03-01). -“The skin of fish: inflammation, ulceration and immune response against bacteria. Phytotherapy and nanoparticles as possible treatments ” (grant number AGL2014- 51839-C5-1-R). The PhD has been also supported by the Spanish Ministry of Economy and Competitiveness (MINECO) with a PhD grant number BES-2012-052742 and two short stay grants (numbers EEBB-I-15-09235 to stay at University of New Mexico in USA and EEBB-1-2016-10533 to stay at Nord University in Norway) as well as by the University of Murcia with a Lifelong Learning Programme Erasmus grant to stay at the University of Nordland (Norway). The following persons (in alphabetical order) have been partially participants of the present dissertation: -Alberto Cuesta , Lecturer, University of Murcia. -Diana Ceballos , PhD student, University of Murcia. -José Meseguer , Emeritus Professor, University of Murcia. -María Ángeles Esteban , Professor, University of Murcia. -Monica F. Brinchmann, Associate Professor, Nord University. -Patricia Morcillo , PhD, University of Murcia. Publications related to the present Thesis (7): Cordero H , Ceballos-Francisco D, Cuesta A, Esteban MA. Dorso-ventral skin characterization of farmed fish gilthead seabream ( Sparus aurata ). 2016, submitted. Cordero H , Mauro M, Cuesta A, Cammarata M, Esteban MA. In vitro cytokine profile revealed differences from dorsal and ventral skin susceptibility to pathogen-probiotic interaction in gilthead seabream. Fish & Shellfish Immunology 2016, 56: 188-191. Cordero H , Cuesta A, Meseguer J, Esteban MA. Characterization of the gilthead seabream ( Sparus aurata ) immune response under a natural lymphocystis virus (LCDV) outbreak. Jornal of Fish Diseases 2016, 39: 1467-1476. Cordero H , Cuesta A, Meseguer J, Esteban MA. Changes in the levels of humoral immune activities after storage of gilthead seabream ( Sparus aurata ) skin mucus. Fish & Shellfish Immunology 2016, 58: 500-507. Cordero H , Brinchmann MF, Cuesta A, Meseguer J, Esteban MA. Skin mucus proteome map of European sea bass ( Dicentrarchus labrax). Proteomics 2015, 23-24: 4008-4020. Cordero H , Morcillo P, Cuesta A, Brinchmann MF, Esteban MA. Differential proteome profile of skin mucus of gilthead seabream ( Sparus aurata ) after probiotic intake and/or overcrowding stress. Journal of Proteomics 2016, 132: 41-50. Cordero H , Brinchmann MF, Cuesta A, Esteban MA. Chronic wounds alter the proteome profile in skin mucus of farmed fish gilthead seabream. In preparation. Another publications/collaborations (11): Cordero H , Guardiola FA, Tapia-Paniagua ST, Cuesta A, Meseguer J, Balebona MC, Moriñigo MA, Esteban MA. Modulation of immunity and gut microbiota after dietary administration of alginate encapsulated Shewanella putrefaciens Pdp11 to gilthead seabream ( Sparus aurata L.). Fish & Shellfish Immunology 2015, 45: 608-618. Cordero H , Morcillo P, Meseguer J, Cuesta A, Esteban MA. Effects of Shewanella putrefaciens on innate immunity and cytokine expression profile upon high stocking density of gilthead seabream specimens. Fish & Shellfish Immunology 2016, 51: 33-40. Cordero H , Guzmán-Villanueva LT, Chaves-Pozo E, Arizcun M, Ascencio-Valle F, Cuesta A, Esteban MA. Comparative ontogenetic development of two marine teleosts, gilthead seabream and European sea bass: new insights into nutrition and immunity. Developmental and Comparative Immunology 2016, 65: 1-7. Morcillo P, Cordero H , Meseguer J, Esteban MA, Cuesta A. Toxicological in vitro effects of heavy metals on gilthead seabream ( Sparus aurata L.) head-kidney leucocytes. Toxicology In Vitro 2015, 30: 412-420. Esteban MA, Cordero H , Martínez-Tomé M, Jiménez-Monreal AM, Bakhrouf A, Mahdhi A. Effect of dietary supplementation of probiotics and palm fruits extracts on the antioxidant enzyme gene expression in the mucosae of gilthead seabream ( Sparus aurata L.). Fish & Shellfish Immunology 2014, 39: 532-540. Morcillo P, Cordero H , Meseguer J, Esteban MA, Cuesta A. In vitro immunotoxicological effects of heavy metals on European sea bass ( Dicentrarchus labrax L.) head-kidney leucocytes. Fish & Shellfish Immunology 2015, 47: 245-254. Trapani A, Mandracchia A, Di Franco C, Cordero H , Morcillo P, Comparelli R, Cuesta A, Esteban MA. In vitro characterization of 6-coumarin loaded solid lipid nanoparticles and their uptake by immunocompetent fish cells. Colloids and Surfaces B 2015, 127: 79-88. Guzmán-Villanueva LT, Tovar-Ramírez D, Gisbert E, Cordero H , Guardiola FA, Cuesta A, Meseguer J, Ascencio-Valle F, Esteban MA. Dietary administration of b- 1,3/1,6-glucan and probiotic strain Shewanella putrefaciens , single or combined, on gilthead seabream growth, immune responses and gene expression. Fish & Shellfish Immunology 2014, 39: 34-41. Tapia-Paniagua ST, Vidal S, Lobo C, Prieto-Álamo MJ, Jurado J, Cordero H , Cerezuela R, García-De La Banda I, Esteban MA, Balebona MC, Moriñigo MA. The treatment with the probiotic Shewanella putrefaciens Pdp11 of specimens of Solea senegalensis exposed to high stocking densities to enhance their resistance to disease. Fish & Shellfish Immunology 2014, 41: 209-221. González-Silvera D, Guardiola FA, Cordero H , Cuesta A, Esteban MA, Martínez- López FJ, López-Jiménez JA. The short-term effects of farmed fish food consumed by wild fish congregating outside the farms. Marine Pollution Bulletin 2016, doi: 10.1016/j.marpolbul.2016.10.055 . Hoseinifar SH, Khalili M, Rufchaei R, Raeisi M, Attar M, Cordero H , Esteban MÁ. Effects of date palm fruit extracts on skin mucosal immunity, immune related genes expression and growth performance of common carp ( Cyprinus carpio ) fry. Fish & Shellfish Immunology 2015, 47: 706-711. Selected scientific communications in international conferences (7) Cordero H , Morcillo P, Buonocore F, Meseguer J, Cuesta A, Esteban MA. Apoptotic effects of inorganic arsenic exposure on European sea bass ( Dicentrarchus labrax ). Oral Communication in VI Iberian Congress of Ichthyology, Murcia, June 21-24, 2016. Cordero H , Morcillo P, Cuesta A, Brinchmann MF, Esteban MA. Proteome of gilthead seabream ( Sparus aurata ) skin mucus after probiotic feeding and crowding stress. Oral Communication in the 17th International Conference on Diseases of Fish and Shellfish, Las Palmas, September 7-11, 2015. Cordero H , Guzmán Villanueva LT, Chaves-Pozo E, Tovar-Ramírez D, Ascencio-Valle F, Cuesta A, Esteban MA. Comparative ontogenetic development of two marine teleosts, gilthead seabream (Sparus aurata ) and European sea bass ( Dicentrarchus labrax ). Poster Communication in the 13th International Society of Developmental and Comparative Immunology Congress, Murcia, June 28-July 3, 2015. Cordero H , Brinchmann M, Cuesta A, Meseguer J, Esteban MA. Skin mucus proteome map of European sea bass ( Dicentrachus labrax ): a non- invasive technique for the search of immune biomarkers. Oral Communication in the 3rd International Work-Conference on Bioinformatics and Biomedical Engineering, Granada, April 15-17, 2015. Cordero H , Morcillo P, Guardiola FA, Cuesta A, Meseguer J, Esteban MA. LCDV increases the cellular immune response of gilthead seabream ( Sparus aurata ). Poster Communication in the 9th International Symposium on Viruses of Lower Vertebrates, Málaga, October 1-4, 2014. Cordero H , Mahdhi A, Guardiola FA, Meseguer J, Bakhrouf A, Esteban MA. Effect of two probiotics and date palm extract on skin and gut gene expression of gilthead seabream ( Sparus aurata L.). Poster Communication in the 7th Probiotics, Prebiotics & New Foods, Rome, September 8-10, 2013. Cordero H , Guardiola FA, Meseguer J, Cuesta A, Esteban MA. Effect of probiotic Shewanella putrefaciens on skin gene expression of gilthead seabream (Sparus aurata L.). Poster Communication in the First International Conference of Fish and Shellfish Immunology, Vigo, June 25 to 28, 2013. Chapters of book (1) Cordero H , Esteban MA, Cuesta A. Use of probiotic bacteria against bacterial and viral infections in shellfish and fish aquaculture. In: Sustainable Aquaculture Techniques, Hernández-Vergara, M (Ed.), InTech, doi: 10.5772/57198 . Other merits Organizer of VI Iberian Congress of Ichthyology, Murcia, June 21-24, 2016. Member of group B of the commission for the Degree in Biology (2016). Representative of doctoral students in Molecular Biology and Biotechnology from the University of Murcia for 3 years (2014-2016). Index Index Index I Abbreviations V List of figures XV List of tables XX Graphical abstract XXV Summary 1 Introduction 7 1.1 Overview of the immune system of teleosts 9 1.2 Skin mucosal immunity of teleosts 16 1.3 Omics and their applications in skin mucus of teleosts 19 Objectives 27 Experimental chapters 31 Chapter I - Characterization of gilthead seabream skin: dorso-ventral 33 differentiation Abstract 34 Introduction 35 Materials and Methods 36 Results and Discussion 41 Chapter II - Gilthead
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