Certain Aquatic Eukaryotes Harbor an OLD-Like Immune Defense System

Recent investigations have unveiled the existence of an ancient immune defense system, reminiscent of prokaryotic anti-phage defense mechanisms, within certain aquatic eukaryotes. The Overcoming Lysogenization Defect (OLD) defense system, thoroughly studied in prokaryotes, was previously unrecognized in eukaryotes. This study identifies old-like genes in various aquatic eukaryotes, including the SAR supergroup, Filasterea, Chytridiomycota, and several metazoan lineages such as Placozoa, Cnidaria, Spiralia, Hemichordata, and Cephalochordata.

It is noteworthy that molluscs exhibit old-like genes in bivalves but not in gastropods and cephalopods. Intriguingly, the filasterean Capsaspora owczarzaki, an endosymbiont of the gastropod Biomphalaria glabrata, encodes possible secreted OLD-like proteins, implying it could offer its host symbiont-mediated antiviral protection.

Genome and transcriptome analyses revealed that old-like genes differ in copy number and intron count and are expressed in certain eukaryotic lineages. Despite retaining key structural features, these OLD-like proteins have a distinct topology compared to their prokaryotic counterparts. Structural predictions suggest homodimeric dsDNA-bound architectures similar to those of the Bacillus cereus VD045 GajA OLD homodimer in bacteria.

Phylogenetic analysis categorized OLD-like proteins into three distinct clusters, one of which potentially traces back to an ancient inheritance from the ancestral Promethearchaeota (formerly Asgard archaea) host. These discoveries underscore the unexpected presence of old-like genes in specific aquatic eukaryotes, shedding fresh light on their evolutionary history and potential role in antiviral defense mechanisms.