The cellular, chemical, and molecular response of the sponge Aplysina aerophoba to grazing

Sponges (Phylum Porifera) are sessile invertebrates that produce secondary metabolites to defend against predators, competition and bio-fouling. Nevertheless, certain sea slugs (Phylum Mollusca: Class Opistobranchia) have specialized in grazing on specific sponge species, which leaves the sponge tissue exposed. To date, no study has examined the response of sponges upon grazing. In the present PhD thesis, I investigated the Mediterranean sponge Aplysina aerophoba which produces brominated alkaloids with antibacterial and deterrence properties against generalist predators. These brominated compounds are enriched in a particular cell type, so-called spherulous cells. However, A. aerophoba is the main food source for a specialist grazer – the sea slug Tylodina perversa – which tolerates brominated compounds and also exploits them for its own defense. By ways of microscopic technologies, MALDI-imaging MS, and RNA-Seq, I aimed to investigate the cellular processes, the potential role of secondary metabolites, and molecular mechanisms in the response of the sponge to grazing. I hypothesized that grazing can induce signaling pathways for a recruitment of spherulous cells with secondary metabolites. Three treatments were applied: control, grazing, and mechanical damage. Samples were collected 3 hours, 1 day, 3 days, and 6 days after treatment. My results showed that spherulous cells were recruited to the wounded site in a time-dependent manner. MALDI-imaging MS showed that both brominated compounds (aerophobin-2 and aeroplysinin-1) localized usually at the sponge surface and accumulated at the damaged surface upon wounding. The expression of key potential candidate genes for cell migration, wound sealing, and immune response were activated also in a time-dependent manner based on RNA-Seq data. Compared to mechanical damage, grazing triggered a relatively lower degree of stimulus perception, inflammatory response, and oxidative stress, and induced a relatively higher degree of chemical perception, phagocytosis, and mucus production. As spherulous cells are common in many members of the class Demospongiae, the recruitment of defensive cells may also occur in other sponges for protecting these filter-feeders. My PhD thesis contributes to understanding the evolutionary mechanisms in sponges for facing grazing and wounding.


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