Schiano, Valentina (2022) "Effects of caulerpin, a metabolite isolated from invasive algae, on zebrafish trophic behaviour and reproductive performance”. [Tesi di dottorato]

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Biological invasions are widely recognized as a growing threat to the integrity of most terrestrial and marine ecosystems on Earth. The theme is of great concern for marine ecosystems and, in particular, for the Mediterranean Sea, which is considered a major hotspot of marine invasions. Invasive species can modify habitats and community composition, may cause local extinctions and the loss of native genotypes, damaging ecosystem processes and functioning. In addition, recent studies emphasize that bioactive compounds from marine invasive species may exert unexpected and dramatic impacts on the native communities, acting as drivers of changes in marine ecosystems. In this framework, the green macroalga Caulerpa cylindracea has come to the fore due to its high invasiveness in the Mediterranean. Actually, this alga forms impenetrable monocultures that negatively affect native seaweeds and seagrasses and the livelihoods of local fishermen. Moreover, the alga has become a favorite food of native fish, including the edible white sea bream Diplodus sargus, which changed its alimentary habits by feeding almost exclusively on C. cylindracea. The novel diet was correlated with alterations in metabolic pathways, suggesting possible chemically-mediated detrimental effects of the new diet. However, the potential negative impact of specific bioactive metabolites from C. cylindracea on fish health remains still unclear. One of its secondary metabolites, the bisindolic alkaloid caulerpin (CAU), has already attracted the attention of the scientific community for its properties of pharmacological interest. Furthermore, recent studies have shown that CAU acts as peroxisome proliferator-activated receptor (PPAR) α/γ agonist and that it accumulates in the tissues of fish feeding on the alga. These findings led to hypothesize an involvement of CAU in the control of the main pathways responsible of fish health. The study object of this thesis tried to investigate the effect of a CAU-based diet in the control of appetite, metabolic and reproductive pathways, using zebrafish as an animal model. Obtained results showed a general health improvement in fish treated with CAU, with an increase of appetite and reproductive performance, significantly increasing both fertility and embryos/larvae viability. These effects were in turn associated with CAU-mediated transcriptional induction of genes involved in the control of food intake and regulation of lipid metabolism. The analysis of the fatty acid composition of fish muscle also showed a positive effect of CAU on the quantity and quality of the fats present in the white muscle of treated fish. On the other hand, CAU effects also included the positive control of the hypothalamus-pituitary-gonadal axis. Actually, in both sexes the master genes involved in reproduction were up-regulated in the brain under the effects of dietary CAU, in turn associated with overexpression of biosynthetic genes encoding sexual hormones. Morphological analyses showed more differentiated ovary and testis in CAU-treated fish, as supported by the analysis of the genes involved in the reproductive process that appeared down-regulated in the ovary, due to its completely differentiation, and up-regulated in testis in which spermatogenesis is a continuous process. In conclusion, the results of this study suggest that other algal metabolites (e.g. the toxic sesquiterpene caulerpenyne) could be responsible for the adverse effects of a Caulerpa-based diet on Mediterranean fish. Instead, the positive effects of CAU on fish appetite and reproduction pave the way for a possible future desirable valorization of C. cylindracea as a source of bioactive compounds able to improve fish fertility and health.

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