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.
Highlights
Microalgae represent a promising source of biomass feedstock for fuels and chemicals because many species possess the ability to grow rapidly and synthesize large amounts of storage neutral lipids in a form of triacylglycerol (TAG) from sunlight and carbon dioxide
We present five new genomes of the oleaginous microalgae Nannochloropsis spp. that allow genus, species- and strain-level genomic comparison
The eleven type II acylCoA: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
Summary
Microalgae represent a promising source of biomass feedstock for fuels and chemicals because many species possess the ability to grow rapidly and synthesize large amounts of storage neutral lipids in a form of triacylglycerol (TAG) from sunlight and carbon dioxide. Nannochloropsis is a genus of unicellular photosynthetic microalgae in the class Eustigmatophyceae, ranging in size from 2–5 mm and widely distributed in marine, fresh and brackish waters. They are of interest as a potential feedstock for fuels and high-value products because they tolerate broad enivronmental and culture conditions while growing rapidly and producing large amounts of TAG and eicosapentaenoic acid, a high-value polyunsaturated fatty acid [3]. A homologous recombination–based gene transformation system was recently established in Nannochloropsis [4], making trait improvement in this organism possible for overproduction of biomass or desirable products
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