Integrative taxonomy of sponges and cnidarians at "El Pelado" marine protected area (Santa Elena), Ecuador: Assessing the potential of metabolomics
Jaramillo Aguilar, Karla Belén
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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 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. The explorations of our marine biodiversity have not been completed and because the extinction of marine species is becoming alarming with the climate change, I believe similar works should be continued in underexplored regions of our planet. Through this work, I highlighted the importance of an integrative taxonomy approach combining molecular data with key phenotypic traits like the morphological characters and the specialised metabolites for a more precise identification of marine invertebrates. Even if these preliminary metabolomic studies are highly promising, the variability with time and space of the metabolome still needs to be assessed before expanding the use of this new tool for taxonomy.
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