Horizontal Gene Transfer and Fusion Spread Carotenogenesis Among Diverse Heterotrophic Protists

Thraustochytrids (phylum: Labyrinthulomycota) are nonphotosynthetic marine protists. Some thraustochytrids have crtIBY, a trifunctional fusion gene encoding a protein capable of beta-carotene biosynthesis from geranylgeranyl pyrophosphate. Here we show that crtIBY is essential in, and encodes the sole pathway for, carotenoid biosynthesis in the thraustochytrid Aurantiochytrium limacinum ATCC MYA-1381. We explore the evolutionary origins of CrtIBY and discover that the closest related protein domains are present in a small but diverse group of other heterotrophic protists, including the apusomonad Thecamonas trahens and the dinoflagellates Oxyrrhis marina and Noctiluca scintillans. Each organism within this cluster also contains one or more beta-carotene 15-15 ' oxygenase genes (blh and rpe65), suggesting that the acquisition of beta-carotene biosynthesis genes may have been related to the production of retinal. Our findings support a novel origin of eukaryotic (apo)carotenoid biosynthesis by horizontal gene transfer from Actinobacteria, Bacteroidetes, and/or Archaea. This reveals a remarkable case of parallel evolution of eukaryotic (apo)carotenogenesis in divergent protistan lineages by repeated gene transfers.

Automated summary

In this study, the essential role of the crtIBY gene in carotenoid biosynthesis in the marine protist Aurantiochytrium limacinum ATCC MYA-1381 was demonstrated. The related protein domains were found in other heterotrophic protists, suggesting a horizontal gene transfer event. This reveals a novel origin of eukaryotic (apo)carotenogenesis through parallel evolution in divergent protist lineages.