Multiomics analysis reveals a distinct mechanism of oleaginousness in the emerging model alga Chromochloris zofingiensis

Abstract

Chromochloris zofingiensis, featured due to its capability to simultaneously synthesize triacylglycerol (TAG) and astaxanthin, is emerging as a leading candidate alga for production uses. To better understand the oleaginous mechanism of this alga, we conducted a multiomics analysis by systematically integrating timeresolved transcriptomes, lipidomes and metabolomes in response to nitrogen deprivation. The data analysis unraveled the distinct mechanism of TAG accumulation, which involved coordinated stimulation of multiple biological processes including supply of energy and reductants, carbon reallocation from protein and starch, and 'pushing' and 'pulling' carbon to TAG synthesis. Unlike the model alga Chlamydomonas, de novo fatty acid synthesis in C. zofingiensis was promoted, together with enhanced turnover of both glycolipids and phospholipids, supporting the drastic need of acyls for TAG assembly. Moreover, genomewide analysis identified many key functional enzymes and transcription factors that had engineering potential for TAG modulation. Two genes encoding glycerol-3-phosphate acyltransferase (GPAT), the first committed enzyme for TAG assembly, were found in the C. zofingiensis genome; in vivo functional characterization revealed that extrachloroplastic GPAT instead of chloroplastic GPAT played a central role in TAG synthesis. These findings illuminate distinct oleaginousness mechanisms in C. zofingiensis and pave the way towards rational manipulation of this alga to becone an emerging model for trait improvements.

Novel insights into salinity-induced lipogenesis and carotenogenesis in the oleaginous astaxanthin-producing alga Chromochloris zofingiensis: a multi-omics study

“…2). This is different from nitrogen starvation (ND) treatment, where protein exhibited an immediate decrease [15]. Starch, the major carbohydrate reserve, maintained its content during the early treatment and decreased thereafter ( Fig.…”

“…It has been reported in algae that membrane lipids undergo turnover to provide fatty acyls for TAG assembly under abiotic stress conditions such as nitrogen deficiency (ND) [15,[50][51][52][53][54]. Similarly, salt stress also caused a decrease in polar lipids, but predominantly in the chloroplastic membrane lipids (MGDG, DGDG, SQDG and PG) (Figs.…”

“…3f; Additional file 6: Data S4). According to Liu et al [15], the DEGs were also manually categorized into 12 groups ( Fig. 3g; Additional file 7: Data S5).…”

“…Chromochloris zofingiensis, also referred to as Chlorella zofingiensis, is a freshwater green alga capable of growing robustly under multiple trophic conditions, reaching up to 10 and 100 g L −1 for photoautotrophic and heterotrophic modes, respectively [9,11,12,14]. C. zofingiensis synthesizes a high level of intracellular TAG (up to 50% dry weight) and has been cited as a potential feedstock for biodiesel [11,12,14,15]. The alga is also able to synthesize high-value ketocarotenoids and is thought to be a candidate astaxanthin producer alternative to Haematococcus pluvialis [16].…”

“…By contrast, the effect of salt stress on TAG synthesis by the alga remains to be evaluated. Recently, several transcriptomic studies have been performed for C. zofingiensis under the conditions of nitrogen deprivation, high light and glucose feeding [15,18,24,30], contributing to the understanding of biosynthesis of TAG and/or astaxanthin. However, the data under salt stress conditions are still lacking for C. zofingiensis and the underlying mechanisms are yet to be disclosed.…”