Metabolomic profiling reveals deep chemical divergence between two morphotypes of the zoanthid Parazoanthus axinellae

Metabolomics has recently proven its usefulness as complementary tool to traditional morphological and genetic analyses for the classification of marine invertebrates. Among the metabolite-rich cnidarian order Zoantharia, Parazoanthus is a polyphyletic genus whose systematics and phylogeny remain controversial. Within this genus, one of the most studied species, Parazoanthus axinellae is prominent in rocky shallow waters of the Mediterranean Sea and the NE Atlantic Ocean. Although different morphotypes can easily be distinguished, only one species is recognized to date. Here, a metabolomic profiling approach has been used to assess the chemical diversity of two main Mediterranean morphotypes, the "slender" and "stocky" forms of P. axinellae. Targeted profiling of their major secondary metabolites revealed a significant chemical divergence between the morphotypes. While zoanthoxanthin alkaloids and ecdysteroids are abundant in both morphs, the "slender" morphotype is characterized by the presence of additional and bioactive 3,5-disubstituted hydantoin derivatives named parazoanthines. The absence of these specific compounds in the "stocky" morphotype was confirmed by spatial and temporal monitoring over an annual cycle. Moreover, specimens of the "slender" morphotype are also the only ones found as epibionts of several sponge species, particularly Cymbaxinella damicornis thus suggesting a putative ecological link.