The presence of plasmenyl ether lipids in Capsaspora owczarzaki suggests a premetazoan origin of plasmalogen biosynthesis in animals

Abstract

Plasmalogens are glycerophospholipids with a vinyl ether bond, rather than an ester bond, at sn-1 position. These lipids were described in anaerobic bacteria, myxobacteria, animals and some protists, but not in plants or fungi. Anaerobic and aerobic organisms synthesize plasmalogens differently. The aerobic pathway requires oxygen in the last step, which is catalyzed by PEDS1. CarF and TMEM189 were recently identified as the PEDS1 from myxobacteria and mammals, which could be of valuable use in exploring the distribution of this pathway in eukaryotes. We show the presence of plasmalogens in Capsaspora owczarzaki, one of the closest unicellular relatives of animals. This is the first report of plasmalogens in non-metazoan opisthokontas. Analysis of its genome revealed the presence of enzymes of the aerobic pathway. In a broad BLAST search, we found PEDS1 homologs in Opisthokonta and some genera of Amoebozoa and Excavata, consistent with the restricted distribution of plasmalogens reported in eukaryotes. Within Opisthokonta, PEDS1 is limited to Filasterea (Capsaspora and Pigoraptor), Metazoa and a small group of fungi comprising three genera of ascomycetes. A phylogenetic analysis of PEDS1 traced the acquisition of plasmalogen synthesis in animals to a filasterean ancestor and suggested independent acquisition events for Amoebozoa, Excavata and Ascomycetes.