Horizontal gene transfer and diploidy illuminate evolution and stress adaptation in oleaginous Scenedesmaceae (Chlorophyta)

Oleaginous microalgae combine high lipid content with the ability to grow under diverse environmental conditions, the oleaginous species of family Scenedesmaceae (Sphaeropleales, Chlorophyta) having emerged as a promising source for biofuels, biostimulants, and bioremediation. This study provides long-read genome sequencing of 38 species/strains of Scenedesmaceae, including 16 chromosome-level genome assemblies, to explore the genomic underpinnings of the exceptional adaptive properties of their vegetative cells. Gene family analysis identifies ‘core’ and ‘dispensible’ orthogroups in the Scenedesmaceae and unveils orthogroup expansions and gains in four major metabolic processes that enhance survival of cells under stress: lipid metabolism, sulfur metabolism, resistance to oxidative stress, and heterotrophy. We discover orthogroup gains by horizontal gene transfer (HGT) from non-viridiplant donors in all four processes. Additionally, we identify ten diploid strains, which likely evolved by fusion of gametes and vegetative growth of the diploid cells. We hypothesize that HGT and diploidy fostered adaptive processes in the Scenedesmaceae. Oleaginous microalgae can grow in wastewater and have potential applications in biotechnology and bioremediation. This analysis of the genomes of 38 strains of Scenedesmaceae reveals that horizontal gene transfer and diploidy likely fostered evolution of their unique properties and survival under stress.