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Integrating transcriptomic and metabolomic analysis of the oleaginous yeast Rhodosporidium toruloides IFO0880 during growth under different carbon sources

Abstract

Rhodosporidium toruloides is an oleaginous yeast capable of producing a variety of biofuels and bioproducts from diverse carbon sources. Despite numerous studies showing its promise as a platform microorganism, little is known about its metabolism and physiology. In this work, we investigated the central carbon metabolism in R. toruloides IFO0880 using transcriptomics and metabolomics during growth on glucose, xylose, acetate, or soybean oil. These substrates were chosen because they can be derived from plants. Significant changes in gene expression and metabolite concentrations were observed during growth on these four substrates. We mapped these changes onto the governing metabolic pathways to better understand how R. toruloides reprograms its metabolism to enable growth on these substrates. One notable finding concerns xylose metabolism, where poor expression of xylulokinase induces a bypass leading to arabitol production. Collectively, these results further our understanding of central carbon metabolism in R. toruloides during growth on different substrates. They may also help guide the metabolic engineering and development of better models of metabolism for R. toruloides.

Key points

Gene expression and metabolite concentrations were significantly changed.

Reduced expression of xylulokinase induces a bypass leading to arabitol production.

R. toruloides reprograms its metabolism to allow growth on different substrates.

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Data availability

RNA sequencing reads are uploaded to a NCBI bioproject (Accession number: PRJNA660884). Additional datasets are uploaded at the research group github page: https://github.com/raogroupuiuc/rt88_growth. Other datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Acknowledgements

We thank Hoang Dinh for helpful discussions. We thank Dr. Christopher J. Fields and Dr. Jenny Drnevich, affiliated with High-performance Computing in Biology (HPCBio) at University of Illinois at Urbana-Champaign, for their help with the initial RNAseq data analysis. This material is based upon the work supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research under Award Numbers DE-SC0018420 and DE-SC0018260.

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SJ, YJ, and CR conceived the project. SJ, AD, JL, EY, and HW designed and performed experiments. AD, SJ, JL, EY, and CR analyzed the data. SJ, AD, and CR wrote the manuscript and designed the figures. All authors discussed the results and contributed to the final manuscript.

Corresponding author

Correspondence to Christopher V. Rao.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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The authors declare no competing interests.

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Sujit Sadashiv Jagtap and Anshu Deewan are Equal Contribution

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Jagtap, S.S., Deewan, A., Liu, JJ. et al. Integrating transcriptomic and metabolomic analysis of the oleaginous yeast Rhodosporidium toruloides IFO0880 during growth under different carbon sources. Appl Microbiol Biotechnol 105, 7411–7425 (2021). https://doi.org/10.1007/s00253-021-11549-8

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  • DOI: https://doi.org/10.1007/s00253-021-11549-8

Keywords

  • Rhodosporidium toruloides
  • Oleaginous yeast
  • Metabolism
  • Transcriptomics
  • Metabolomics
  • Xylulokinase