Genomic Foundation of Starch-to-Lipid Switch in Oleaginous Chlorella spp.
The ability to rapidly switch the intracellular energy storage form from starch to lipids is an advantageous trait for microalgae feedstock. To probe this mechanism, we sequenced the 56.8-Mbp genome of Chlorella pyrenoidosa FACHB-9, an industrial production strain for protein, starch, and lipids. The genome exhibits positive selection and gene family expansion in lipid and carbohydrate metabolism and genes related to cell cycle and stress response. Moreover, 10 lipid metabolism genes might be originated from bacteria via horizontal gene transfer. Transcriptomic dynamics tracked via messenger RNA sequencing over six time points during metabolic switch from starch-rich heterotrophy to lipid-rich photoautotrophy revealed that under heterotrophy, genes most strongly expressed were from the tricarboxylic acid cycle, respiratory chain, oxidative phosphorylation, gluconeogenesis, glyoxylate cycle, and amino acid metabolisms, whereas those most down-regulated were from fatty acid and oxidative pentose phosphate metabolism. The shift from heterotrophy into photoautotrophy highlights up-regulation of genes from carbon fixation, photosynthesis, fatty acid biosynthesis, the oxidative pentose phosphate pathway, and starch catabolism, which resulted in a marked redirection of metabolism, where the primary carbon source of glycine is no longer supplied to cell building blocks by the tricarboxylic acid cycle and gluconeogenesis, whereas carbon skeletons from photosynthesis and starch degradation may be directly channeled into fatty acid and protein biosynthesis. By establishing the first genetic transformation in industrial oleaginous C. pyrenoidosa, we further showed that overexpression of an NAD(H) kinase from Arabidopsis (Arabidopsis thaliana) increased cellular lipid content by 110.4%, yet without reducing growth rate. These findings provide a foundation for exploiting the metabolic switch in microalgae for improved photosynthetic production of food and fuels.
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Jianhua
J
Fan
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Kang
K
Ning
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Xiaowei
X
Zeng
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Yuanchan
Y
Luo
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Dongmei
D
Wang
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Jianqiang
J
Hu
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Jing
J
Li
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Hui
H
Xu
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Jianke
J
Huang
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Minxi
M
Wan
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Weiliang
W
Wang
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Daojing
D
Zhang
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Guomin
G
Shen
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Conglin
C
Run
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Junjie
J
Liao
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Lei
L
Fang
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Shi
S
Huang
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Xiaoyan
X
Jing
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Xiaoquan
X
Su
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Anhui
A
Wang
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Lili
L
Bai
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.).
Zanmin
Z
Hu
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.) ygli@ecust.edu.cn xujian@qibebt.ac.cn.
Jian
J
Xu
State Key Laboratory of Bioreactor Engineering, East China University of Science and Technology, Shanghai 200237, China (J.F., Y.Lu., H.X., J.Hua., M.W., W.W., D.Z., G.S., C.R., J.Lia., L.F., Y.Li.);Single-Cell Center, Chinese Academy of Sciences Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of Sciences, Qingdao, Shandong 266101, China (K.N., X.Z., D.W., J.Hu., J.Li., S.H., X.J., X.S., A.W., J.X.); andInstitute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, China (L.B., Z.H.) ygli@ecust.edu.cn xujian@qibebt.ac.cn.
Yuanguang
Y
Li
D001483:Base Sequence; D050260:Carbohydrate Metabolism; D002244:Carbon / Q000378:metabolism; D002708:Chlorella / Q000235:genetics / Q000378:metabolism*; D002952:Citric Acid Cycle; D004579:Electron Transport; D005227:Fatty Acids / Q000378:metabolism; D023281:Genomics; D052836:Heterotrophic Processes; D050356:Lipid Metabolism; D008969:Molecular Sequence Data; D010085:Oxidative Phosphorylation; D010788:Photosynthesis; D017422:Sequence Analysis, DNA; D013213:Starch / Q000378:metabolism*
D005227:Fatty Acids; D002244:Carbon; D013213:Starch