Nannochloropsis Genomes Reveal Evolution of Microalgal Oleaginous Traits

Abstract

Oleaginous microalgae are promising feedstock for biofuels, yet the genetic diversity, origin and evolution of oleaginous traits remain largely unknown. Here we present a detailed phylogenomic analysis of five oleaginous Nannochloropsis species (a total of six strains) and one time-series transcriptome dataset for triacylglycerol (TAG) synthesis on one representative strain. Despite small genome sizes, high coding potential and relative paucity of mobile elements, the genomes feature small cores of ca. 2,700 protein-coding genes and a large pan-genome of >38,000 genes. The six genomes share key oleaginous traits, such as the enrichment of selected lipid biosynthesis genes and certain glycoside hydrolase genes that potentially shift carbon flux from chrysolaminaran to TAG synthesis. The eleven type II diacylglycerol acyltransferase genes ( DGAT-2) in every strain, each expressed during TAG synthesis, likely originated from three ancient genomes, including the secondary endosymbiosis host and the engulfed green and red algae. Horizontal gene transfers were inferred in most lipid synthesis nodes with expanded gene doses and many glycoside hydrolase genes. Thus multiple genome pooling and horizontal genetic exchange, together with selective inheritance of lipid synthesis genes and species-specific gene loss, have led to the enormous genetic apparatus for oleaginousness and the wide genomic divergence among present-day Nannochloropsis. These findings have important implications in the screening and genetic engineering of microalgae for biofuels.

Author Summary

Microalgae are promising feedstock for biofuels. However, the diversity, origin and evolution of oil-producing microalgal genomes in general, and those of their oleaginous traits in particular, remain poorly understood. We present five new genomes of the oleaginous microalgae Nannochloropsis spp. that allow genus-, species- and strain-level genomic comparison. With each Nannochloropsis genome encoding approximately 6,562–9,915 genes, a core genome of ca. 2,700 genes and a large pan-genome of >38,000 genes were found. The genomes share key genetic features such as gene dose expansion of selected nodes in lipid biosynthesis pathways. Evidence of horizontal gene transfers, primarily from bacteria, was found in most of these nodes. However, the eleven type II acyl-CoA:diacylglycerol acyltransferase genes ( DGAT-2),the highest gene dose reported among known organisms, likely originated from three ancient genomes of the secondary endosymbiosis host and the engulfed green and red algae; they were strictly vertically inherited in each of the Nannochloropsis spp. Thus, multiple genome pooling and horizontal genetic exchange have underlain the enormous genetic makeup underlying TAG production in present-day Nannochloropsis.