Transcriptome and physiological analysis of a lutein-producing alga Desmodesmus sp. reveals the molecular mechanisms for high lutein productivity

A green alga Desmodesmus sp. JSC3 is a lutein producer that appears high in lutein production in batch culture under 200 μmol·m− 2·s− 1 condition using 1 g ∙ L− 1 sodium nitrate as nitrogen source. Because lutein content increased as growth advanced with the maximum (5.18 mg ∙ g− 1) on day 6, comparative transcriptome and physiological analyses on day 1, 6, and 8 were thus employed to uncover the molecular mechanisms for lutein production in this lutein producer. The gene set enrichment analysis using the False Discovery Rate (FDR) test showed that chlorophyll synthesis and photosynthesis were significantly changed when lutein accumulated. The up-regulation of the carotenogenesis genes explains the preference of this alga in lutein accumulation by enhancing lycopene synthesis and promoting metabolic flux towards synthesis of α-carotene and then hydroxylation of the β- and ε-ring of α-carotene, in the late exponential growth period (4-6 days). Chlorophyll content and the expression of the genes encoding the enzymes in tetrapyrrole biosynthesis also increased during 0-6 days, although chlorophyll a/chlorophyll b ratio decreased on day 6 due to light attenuation caused by high cell density. Photosynthetic activity and the expression of the genes encoding light-harvesting complex (LHC) proteins increased during 0-4 days but decreased after that due to nitrogen deficiency (up-regulation of high-affinity nitrate transporter gene and low medium nitrate concentration). It suggests that LHC synthesis and photosynthesis are sensitive to nitrogen deficiency occurring on day 6 while pigment synthesis remains active. Because the expression of the genes encoding LHC-like proteins (early light-inducible proteins) that bind lutein and chlorophyll increased on day 6, LHC-like proteins could be temporarily stores of accumulating pigments. In conclusion, coordinate up-regulation of LHC-like proteins with pigment synthesis for the acclimation to decreasing light availability is believed as the molecular mechanism for high lutein production in Desmodesmus sp. JSC3.