Transcriptomic and metabolomic analyses reveal the positive effect of moderate concentration of sodium chloride treatment on the production of β-carotene, torulene, and torularhodin in oleaginous red yeast Rhodosporidiobolus odoratus XQR

Abstract

• Rhodosporidiobolus odoratus is a promising alternative for carotenoid production. • A 0.75 mol/L NaCl treatment significantly increases carotenoid production in R. odoratus . • Upregulated terpenoid backbone, carotenoid, and TCA cycle pathways contribute to the increase. • Salt-stress-induced ROS led to the overproduction of carotenoids for antioxidant purposes. Carotenoids, a family of lipid-soluble pigments, have garnered growing interest for their health-promoting benefits and are widely utilized in the food, feed, pharmaceutical, and cosmetic industries. Rhodosporidiobolus odoratu s, a representative oleaginous red yeast, is considered a promising alternative for producing high-value carotenoids including β-carotene, torulene, and torularhodin. Here, the impact of varying concentrations of NaCl treatments on carotenoid contents in R. odoratus XQR after 120 h of incubation was examined. The results indicated that, as compared to the control (59.37 μg/g dw ), the synthesis of total carotenoids was significantly increased and entirely suppressed under low-to-moderate (0.25 mol/L: 68.06 μg/g dw , 0.5 mol/L: 67.62 μg/g dw , and 0.75 mol/L: 146.47 μg/g dw ) and high (1.0, 1.25, and 1.5 mol/L: 0 μg/g dw ) concentrations of NaCl treatments, respectively. Moreover, the maximum production of β-carotene (117.62 μg/g dw ), torulene (21.81 μg/g dw ), and torularhodin (7.04 μg/g dw ) was achieved with a moderate concentration (0.75 mol/L) of NaCl treatment. Transcriptomic and metabolomic analyses suggested that the increase in β-carotene, torulene, and torularhodin production might be primarily attributed to the up-regulation of some key protein-coding genes involved in the terpenoid backbone biosynthesis ( atoB , HMGCS , and mvaD ), carotenoid biosynthesis ( crtYB and crtI ), and TCA cycle ( pckA , DLAT, pyc, MDH1 , gltA , acnA , IDH1/2 , IDH3 , sucA , sucB , sucD , LSC1 , SDHA , and fumA/fumB ). The present study not only demonstrates a viable method to concurrently increase the production of β-carotene, torulene, torularhodin, and total carotenoids in R. odoratus XQR, but it also establishes a molecular foundation for further enhancing their production through genetic engineering.

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