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Integrative Taxonomy of Sponges and Cnidarians at “El Pelado” Marine Protected Area (Santa Elena) Ecuador: Assessing the Potential of Metabolomics

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Integrative Taxonomy of Sponges and Cnidarians at “El Pelado” Marine Protected Area (Santa Elena) Ecuador: Assessing the Potential of Metabolomics INTEGRATIVE TAXONOMY OF SPONGES AND CNIDARIANS AT “EL PELADO” MARINE PROTECTED AREA (SANTA ELENA) ECUADOR: ASSESSING THE POTENTIAL OF METABOLOMICS By Karla Belén Jaramillo Aguilar A thesis presented for the degree of Doctor of Philosophy Department of Zoology School of Natural Sciences National University of Ireland, Galway December 2019 INTEGRATIVE TAXONOMY OF SPONGES AND CNIDARIANS AT “EL PELADO” MARINE PROTECTED AREA (SANTA ELENA) ECUADOR: ASSESSING THE POTENTIAL OF METABOLOMICS Thesis submitted for the degree of PhD at the National University of Ireland, Galway by PhD candidate: Karla Belén Jaramillo Aguilar Supervisor: Prof. Grace P. McCormack Co-supervisor: Prof. Olivier P. Thomas A thesis submitted to the Zoology Department, Faculty of Science, National University of Ireland, Galway in fulfilment of the requirements of the Degree of Doctor of Philosophy School of Natural Sciences Department of Zoology December 2019 No words can explain the beauty and simplicity of the ocean waves……… they have a peaceful music for those who listen. DECLARATION I declare that this thesis has not been submitted, in whole or in part, to this, or any other University for any degree. Except where otherwise started, this work is the original work of the author. Signed……………………………………. Karla Belén Jaramillo Aguilar Date: 20/12/2019 ACKNOWLEDGMENTS Finally, I have arrived at the final step of this long journey, not only counting the years invested in my PhD studies but also since the beginning of my career as a Marine Biologist. Today I feel very grateful to the life for giving me the opportunity to achieve my childhood dreams of one day become a researcher of the marine life in the oceans. I would like to thank from the depths of my heart to all that people who believed in me and gave me the opportunity to continue developing my career. I would like to thank Prof. Olivier Thomas who believed in my skills and saw my passion for the ocean during the first diving trips in Ecuador and who opened this great opportunity to do a PhD degree. I would like to thank him for his constant support and for being overall an excellent mentor throughout this journey. I wish to express my warm thanks to my supervisor Prof. Grace McCormack for all her advices during my PhD, thank you for showing me how to fight and push myself to get the best of me as a future researcher. I would like also to express my sincere thanks to Prof. Jenny Rodriguez who gave me the opportunity to be part of that beautiful project of marine biodiversity at the prestigious Research Centre CENAIM (National Centre of Aquaculture and Marine Research) ESPOL Polytechnic University and also a big thanks to the heads of CENAIM, Prof. Stanislaus Sonnenholzner, Prof. Bonny Bayot and Ing. Andrés Pedrazzoli, for opening the doors in CENAIM-ESPOL to grow as a future researcher and for providing me all the facilities to complete my PhD during these years. Also, I’m grateful with my PhD examiners Dr. Thierry Pérez and Dr. Michel Dugon for assessing my work. I wish to express my warm thanks to the excellent taxonomists Dr. Frederic Sinniger and Prof. Eduardo Hajdu for sharing with me their valuable knowledge of these lovely groups of marine invertebrates (Sponges and Zoantharians) and also for their patience to teach me all the basis of this hard but beautiful branch of the science that is the taxonomy. I would also like to thank Dr. Gregory Genta-Jouve and Mehdi Bennidir for training me in metabolomics and molecular networking, chemistry tools of which I am today in love today. A big thanks to Maria Miguel for her patient and to be always there supporting me in the hardest moments of this journey. Finally, I would like to thank all my colleagues from the biodiversity team in CENAIM for all their collaboration during the diving expeditions and the hard work to carry out the Biodiversity project in Ecuador. Also, to my colleagues of the Marine Biodiscovery group and of the School of Zoology-Ryan Institute of NUI Galway for all their support and the beautiful moments shared in Ireland. Finally, I cannot forget to thank my parents and my brother, to be always there encouraging me and supporting me with all their love to achieve my goals and to allow make my dreams come true. I II ABSTRACT In the course of the XXI century, the explorations of our oceans have moved towards the extremes with several highly funded projects to inspect remote places like the poles or the deep- sea. Does it mean that inventories of the marine biodiversity have been published for all the coasts of our inhabited continents? The answer to this question is without any doubt no! For instance, the Tropical Eastern Pacific (TEP) has been largely overlooked for its marine biodiversity, apart from the Galapagos Islands and the coasts of central America. No rigorous inventory of the marine invertebrates present in the Guayaquil ecoregion were available at the beginning of my PhD, and only few scientific data have been reported for the diversity in the dominant groups of this area like Porifera, Zoantharia or Alcyonacea. This research work was therefore placed in the context of the first significant project funded by the Ecuadorian government to describe the marine biological and chemical diversity present in a small Marine Protected Area of the Guayaquil ecoregion called Marine Reserve El Pelado (REMAPE). The main objective of this thesis was to collect, describe and inventory common species of the three groups of marine invertebrates cited before and present in this area. To this end, I first used a classical approach combining morphological features and molecular data. Furthermore, as these invertebrates are also known to produce a diversity of metabolites that could find applications for human and animal health, the second objective was to assess the metabolomic fingerprints as a complementary tool for the systematics of these targeted species. In a first instance, sponges were not found as dominant invertebrates in this area placed at the confluence of warm and cold currents, and therefore more propitious for the development of cnidarians. My research was focused on the class Demospongiae present in this area, as the most dominant sponge species in the area from the genus Aplysina (Verongiida) is currently under study by other collegues. A sister species of Callyspongia californica largely distributed in the north of the TEP was found to interact with stony corals (genus Pocillopora) in the REMAPE area. A set of encrusting sponges was then described for the first time throughout of the mainland coast of Ecuador with the outstanding description of a new species named Tedania ecuadoriensis sp. nov. These species were described using morphological and molecular analyses but the metabolomic approach was not applied here as the sponge species belong to very diverse groups and the chance to find common metabolites was limited. The main part of my work was then dedicated to the study of species belonging to a very abundant order of the phylum Cnidaria in this region named Zoantharia (subclass Hexacorallia). A minimum of six species were found and described for the first time along this coast. They include species of the suborder Macrocnemina largely distributed around the El Pelado islet with some of them like Antipathozoanthus hickmani, and Terrazoanthus patagonichus found as epibionts of other dominant cnidarians like black corals or octocorallians. Then species of the III suborder Brachycnemina of the genera Zoanthus and Palythoa were found covering the shallow water of the mainland coast. Even if the molecular data matched the morphological data at the genus level, some uncertainties remained at the species level. I therefore decided to assess the use of the LC-MS metabolomics targeted approach to separate sister species. Some families of natural products were identified as chemical markers for some groups of zoantharians: ecdysteroids and zoanthoxanthin derivatives were found in all the species with terrazoanthines only present in the species Terrazoanthus patagonichus. Zoanthamines were only found in one species of Zoanthus and halogenated tyrosine alkaloids only in both species of the family Parazoanthidae. These families of natural products can represent chemical markers for these groups, but the generality of this rule must be confirmed by other studies on zoantharians from different regions. Importantly, a potentially new species of Terrazoanthus has been identified in this region and its description must be completed. The last and dominant group studied in this area was the order Alcyonacea (Subclass Octocorallia) also known as soft corals. The diversity of this group was found to be extremely high with 12 species studied in this thesis, but this number is for sure underestimated. Here also the molecular data were difficult to obtain and inconclusive in some cases to distinguish some sister species of the genera Pacifigorgia and Muricea for instance. The low resolution of some loci was responsible for the remaining uncertainties and here the untargeted metabolomic approach was fully assessed. The metabolomic approach was found highly conclusive to separate the five genera studied while some uncertainties remained to separate Muricea species. The additional use of molecular networking through MS/MS fragmentation analyses was proved efficient to visualise better the clusters of entire families of metabolites characteristic of the genera. Finally, these first integrative systematic studies of Porifera, Zoantharia and Alcyonacea in the Marine Reserve REMAPE located in the Santa Elena province, mainland Ecuador provided useful information on the distribution of species of these groups throughout the TEP realm. Most of the species were described for the first time in this area together with their molecular and chemical data. Potentially new species of zoantharian and sponges are reported in this work and further studies should certainly lead to additional new species.
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