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Integrating Transcriptomics and Metabolomics to Characterize Metabolic Regulation to Elevated CO2 in Chlamydomonas Reinhardtii

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Abstract

With atmospheric CO2 increasing, a large amount of CO2 is absorbed by oceans and lakes, which changes the carbonate system and affects the survival of aquatic plants, especially microalgae. The main aim of our study was to explore the responses of Chlamydomonas reinhardtii (Chlorophyceae) to elevated CO2 by combined transcriptome and metabolome analysis under three different scenarios: control (CK, 400 ppm), short-term elevated CO2 (ST, 1000 ppm), and long-term elevated CO2 (LT, 1000 ppm). The transcriptomic data showed moderate changes between ST and CK. However, metabolic analysis indicated that fatty acids (FAs) and partial amino acids (AAs) were increased under ST. There was a global downregulation of genes involved in photosynthesis, glycolysis, lipid metabolism, and nitrogen metabolism but increase in the TCA cycle and β-oxidation under LT. Integrated transcriptome and metabolome analyses demonstrated that the nutritional constituents (FAs, AAs) under LT were poor compared with CK, and most genes and metabolites involved in C and N metabolism were significantly downregulated. However, the growth and photosynthesis of cells under LT increased significantly. Thus, C. reinhardtii could form a specific adaptive evolution to elevated CO2, affecting future biogeochemical cycles.

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Abbreviations

CK:

Control

ST:

Short-term acidification

LT:

Long-term acidification

Ppm:

Parts per million

LC:

Low concentrations of CO2

HC:

High concentrations of CO2

UPLC-Q-TOF-MS:

Ultra-performance liquid chromatograph coupled to quadrupole-time of flight mass spectrometry

CCM:

CO2 concentrating mechanism

FPKM:

Fragments per kilobase million mapped reads

GO:

Gene ontology

KEGG:

Kyoto Encyclopedia of Gene and Genomes

PCA:

Principal component analysis

PLS-DA:

Partial least squares-discriminant analysis

OPLS-DA:

Orthogonal projections for latent structures-discriminant analysis

DEG:

Differentially expressed gene

SDM:

Significantly different metabolite

VIP:

Variable importance for the projection

TAG:

Triacylglycerol

FA:

Fatty acid

AA:

Amino acid

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Funding

This research was supported by the National Key Research and Development Program of China (Grant numbers 2018YFD0900703), Major Scientific and Technological Innovation Project of Shandong Provincial Key Research and Development Program under contract 2019JZZY020706, National Natural Science Foundation of China grant (31770393), Financial Fund of the Ministry of Agriculture and Rural Affairs, P. R. of China (NFZX2018), China Agriculture Research System (CARS-50), and Taishan Scholars Funding of Shandong Province.

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Authors and Affiliations

  1. College of Marine Science and Biological Engineering, Qingdao University of Science and Technology, 53 Zhengzhou Road, Qingdao, 266042, China

    Yufei Zhang, Zipeng Gu, Yudong Ren, Lu Wang, Jian Zhang & Chengwei Liang

  2. School of Life Sciences, Ludong University, 186 Hongqi Middle Road, Yantai, 264025, China

    Shanying Tong

  3. Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, 106 Nanjing Road, Qingdao, 266071, China

    Yitao Wang, Dong Xu, Xiaowen Zhang & Naihao Ye

  4. National Oceanographic Center, Qingdao, 266071, China

    Yitao Wang, Dong Xu, Xiaowen Zhang & Naihao Ye

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  1. Yufei Zhang
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  2. Zipeng Gu
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  4. Lu Wang
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  10. Xiaowen Zhang
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Contributions

C.W.L. and N.H.Y. designed the project. Y.F.Z., Z.P.G., Y.D.R., L.W., and J.Z. performed the research. Y.F.Z., C.W.L., S.Y.T., D.X., X.W.Z., and Y.T.W. analyzed the data. Y.F.Z. and C.W.L. wrote the first draft. All authors contributed to interpreting the data and writing the manuscript. The manuscript is approved by all authors for publications. This work is the original works of the authors, and the manuscript was not previously submitted to this journal.

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Correspondence to Chengwei Liang or Naihao Ye.

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Zhang, Y., Gu, Z., Ren, Y. et al. Integrating Transcriptomics and Metabolomics to Characterize Metabolic Regulation to Elevated CO2 in Chlamydomonas Reinhardtii. Mar Biotechnol 23, 255–275 (2021). https://doi.org/10.1007/s10126-021-10021-y

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