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Improvement of water quality and bioproduction of high added-value products from the integrated cultivation of marine sponges in fish aquaculture systems

Varamogianni-Mamatsi Despoina

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Summary

Mariculture, typically supported by marine cage systems, constitutes a significant economic sector for several countries across the world and plays an increasing role in fish supply. During the last decades, a pronounced activity has been reported in the Mediterranean Sea, with Greece being one of the major producers of seabream and seabass finfish worldwide. With the gradual increase of global population, and consequently, the demands for fish and fish-related products, mariculture systems are expected to face an even more unparalleled growth. To enhance productivity, fish farmers currently use larger densities of feed and chemicals that are necessary to ensure the health and growth within the culture. A significant portion of these administered substances remains freely dissolved in the water column, or can either end up as particles in marine sediments, leading to sound threats for aquatic and human life. Unconsumed fish feeds, accompanied by massive excretions of fish faeces and other metabolic waste products are the main cause for nutrient enrichment of water and sediments near fish farms. On the other hand, aggressive administration of therapeutants, such as antibiotics, parasiticides, anesthetics,disinfectants and hormones, or antifouling booster biocides that are used to prevent fouling in submerged production structures, can potentially lead to high organic loadings, chemical pollution and bioaccumulation of contaminants in fish stocks or other marine life. Other pollutants that may occur in fish farm environments include heavy metals and polycyclic aromatic hydrocarbons (PAHs),discharged from offshore and coastal anthropogenic activities. As a result, nutrient and organic pollution can provoke a series of adverse effects, including water deterioration, hypoxia, biological pollution, eutrophication and habitat destruction, with severe economic losses for fish farmers. To alleviate aquaculture pollution through eco-sustainable and socially acceptable manners, integrated multi-trophic aquaculture (IMTA) systems emerge as feasible solution. Such systems combine fish aquaculture with rearing of secondary extractive species, in a way that nutrients and fish wastes are recycled to promote growth of the co-cultured organisms, while the latter present an additional monetary benefit to the enterprise, through their own economic value. Over the years, many organisms have been documented as promising IMTA candidates. Among them, marine sponges stand as excellent candidates, in light of their innate filter-feeding properties and their capability to retain a variety of organic waterborne substances, from particulate to dissolved forms. Besides their high bioremediation capacity for an array of biological and organic pollutants, their biomass is considered a “gold mine”, given their applicability in various biotechnological fields, from bath sponges to bioactive compounds resources. However promising, only few existing studies have conceived the “sponge-drivenbioremediation/bioproduction” concept in aquacultures worldwide, with Greece being practically inactive. Considering the thriving aquaculture sector of Greece and the vast diversity of sponges existing in Aegean Sea, it is essential to gain a better view of the integration potential of native sponge species in fish farms.The aim of this dissertation is to (a) assess the bioremediation capacity of Mediterranean sponges through controlled laboratory experiments involving typical aquaculture biological and chemical pollutants and to (b) explore the valorization potential of candidate sponges through the targeted analysis of known metabolites and bioactivity screening. The cleanup experiments were employed for the four ubiquitous Mediterranean species Agelas oroides, Axinella cannabina, Chondrosia reniformis and Sarcotragus foetidus, which were distinguished for their high natural abundance, variability in body form and satisfactory performance under rearing conditions. The in vitro capability to mitigate aquaculture-related biological pollution was assessed for three phytoplanktonic cells, in an attempt to simulate sponges’ response to eutrophic algal blooms. The tested microalgal substrates were exhibiting different size/motility characteristics and belonged to genera of Nannochloropsis sp. (~3.2 μm, nonmotile), Isochrysis sp. (~3.8 μm, motile), and Phaeodactylum (~21.7 μm, nonmotile). Sponge explants were exposed for 7 h to microalgae-enriched seawater under different experimental setups. First, it was shown that all four candidates were capable of retaining their cleanup capacity across a span of four or five successive days. When exposed to varying cell concentrations approximating the gradient from oligotrophic to highly eutrophic systems, sponges maintained their optimal filtering activity. The same argument was partially true when exposed to different illumination conditions. Different feeding preferences were observed among sponge species for microalgal substrates with distinct size and motility traits. Overall, the study sponges exhibited a wide range of retention efficiencies for the different phytoplankton cells, with the highest average values found for the species A. oroides (70%) and S. foetidus (44%).The same candidate sponges were further investigated for their ability to remove typical aquaculture-related dissolved organic pollutants from seawater. This series of in vitro experiments involved the exposure to (i) individual chemicals belonging to antibiotics (i.e., oxytetracycline), antifouling biocides (i.e., diuron and Irgarol 1051) and polycyclic aromatic hydrocarbons (i.e., 2,6-dimethylnapththalene, phenanthrene), as well as (ii) complex organic mixtures, involving filtrates of fish feed and excreta. All sponges were capable of uptaking the various organic substances, by exhibiting a pronounced preference for lipophilic pollutants. To further support this argument, a strong positive correlation was revealed between sponge’s cleanup capacity and substrate hydrophobicity. Among the examinedsponges, A. oroides demonstrated the greatest filtering performance across an array of dissolved organic substances, with the highest rates reported for the highly lipophilic pollutants. At a later stage, we intended to shed light on the processes dictating dissolved organic matter (DOM) removal by sponges. In all studied species, active pumping was found to play a prominent role in the assimilation of dissolved pollutants. This was explained by the much faster rates exhibited from this mechanism compared to the values derived for passive adsorption of pollutants onto dead sponges’ surface. Finally, the uptaken pollutants were shown to be strongly retained by sponges and they were hardly releasedback to seawater as a result of desorption or sponge excretory mechanisms.The final criterion to assess the suitability of the selected sponge species as components of integrated aquaculture, was the valorization potential of their cultivated biomass. For this reason, the two best-performing species in terms of bioremediation capacity, namely A. oroides and S. foetidus, were selected and further analyzed for targeted known biomolecules and bioactivities. This assessment was performed in specimens subjected to rearing in direct proximity to a fish aquaculture for more than a year, as well as to conspecifics from adjacent sponge populations, to estimate the effect of farming on the natural bioproduction potential. An array of natural products was identified in the extracts of both farmed and wild sponges, with the majority of them belonging to alkaloids, benzenoids, indoles, lipids and polyketides. Metabolomic analysis revealed also species-specific chemical patterns, with A. oroides and S. foetidus extracts dominated by alkaloids and lipids, respectively. More importantly, farmed and wild explants of each species demonstrated similar chemical fingerprints, with the majority of the metabolites showing modest differences in their content and on a sponge mass-normalized basis. Furthermore, farmed sponge extracts presented similar or slightly lower antibacterial activity aga

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