Investigations of the Evolved Molecular Basis for Terpenoid Biosynthesis in Marine Sponges.

Ancestral marine sponges produce terpenoid-based compounds, and recent studies have begun to reveal the genetic basis in some species, including the first report of type I terpene synthases (T1TSs) in a Bubarida sponge Obruta collector. Here, we present a further genomic and functional characterization of terpenoid biosynthesis in the isonitrile terpenoid-rich sponge Acanthella cavernosa by integrating multi-omics with comparative genomic, phylogenetic, and biochemical analyses. We found that A. cavernosa retains the full eukaryotic ancestral mevalonate pathway for terpene precursor biosynthesis. Their single α-domain classical T1TSs form a basal, independently evolved lineage related to plant T1TS α-domains, while UbiA-type TSs drive lineage-specific structural diversification. Notably, in contrast to the clustering of T1TSs with other biosynthetic genes observed in some corals, we did not observe such clustering in the sponge we sequenced, which is consistent with the observation in O. collector. Our findings provide additional evidence for the ancestral origin of metazoan terpenoid biosynthesis and further our understanding of early metazoan adaptive evolution, and facilitate biotechnological exploitation of sponge-derived terpenoids.