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.

Molecular and phylogenetic identification of an oil-producing strain of Nannochloropsis oceanica (Eustigmatophyceae) isolated from the southwestern Atlantic coast (Argentina)

“…2) and 18S rDNA (Fig. 3) Andersen et al (1998), Krienitz et al (1996) and Vieler et al (2012) based on 18S rDNA; by Suda et al (2002) and Cao et al (2013) based on 18S rDNA and rbcL; and by Wang et al (2014) based on 1085 single-copy nuclear orthologous gene sets. This topology is consistent with a morphological difference between the 2 main clades.…”

“…(Rodolfi et al 2009, Pal et al 2011, Bondioli et al 2012, N. gaditana (Simionato et al 2011(Simionato et al , 2013, N. oculata (Van Vooren et al 2012), N. salina (Sforza et al 2012) and N. oceanica (Dong et al 2013, Pal et al 2013, Bongiovani et al 2013, Solovchenko et al 2014. Given the importance of Nannochloropsis as an oleaginous species for biodiesel production, a number of genomic and transcriptomic studies on several species of the genus have been recently published (Radakovits et al 2012, Vieler et al 2012, Wei et al 2013, Starkenburg et al 2014, Wang et al 2014, Carpinelli et al 2013, Hu et al 2014, Li et al 2014.…”

“…Thus, the phylogenetic species concept becomes particularly useful (Andersen et al 1998). Species of Nannochloropsis have been delimited by DNA sequence analysis (Fawley & Fawley 2007) based on nuclear (18S rDNA) and chloroplastic (rbcL) markers and sets of orthogonal genes (Krienitz et al 1996, Andersen et al 1998, Suda et al 2002, Vieler et al 2012, Cao et al 2013, Wang et al 2014.…”

Choreography of Transcriptomes and Lipidomes ofNannochloropsisReveals the Mechanisms of Oil Synthesis in Microalgae

“…In C. reinhardtii, the excess photosynthetically fixed carbons and energy are mainly stored in the form of starch and to a much lesser extent TAG under high light or under high light plus N depletion (Buléon et al, 1997;Li et al, 2010aLi et al, , 2010b. In oleaginous microalgae (e.g., Nannochloropsis spp), TAG is the main carbon and energy reserve along with smaller amounts of the water-soluble polysaccharide chrysolaminarin under stress conditions (Radakovits et al, 2012;Vieler et al, 2012;Wang et al, 2014). The genetic makeup and molecular mechanisms that bestow oleaginous microalgae the ability to produce extraordinary amounts of TAG in response to stress remain to be elucidated.…”

“…Nannochloropsis species/strains are of industrial interest due to their ability to grow rapidly, synthesize large amounts of TAGs and high-value polyunsaturated FAs (e.g., eicosapentaenoic acid), and tolerate broad environmental and culture conditions (Sukenik, 1991;Wang et al, 2012). Recently, the genomes of multiple species of Nannochloropsis have been sequenced and partially annotated (Radakovits et al, 2012;Vieler et al, 2012;Wei et al, 2013;Wang et al, 2014). Several transcriptomic analyses have also been conducted with Nannochloropsis (Vieler et al, 2012;Carpinelli et al, 2013;Zheng et al, 2013); however, the individual-snapshot mRNA analyses, which tested only one or two time points, has failed to capture the temporal dynamics of gene expression.…”