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Mitochondrial Citrate Transport System in the Fungus Mucor circinelloides: Identification, Phylogenetic Analysis, and Expression Profiling During Growth and Lipid Accumulation

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Abstract

The mitochondrial citrate transport system, composed of citrate and malate transporters (MTs), can regulate the citrate efflux from mitochondria to cytosol, and then citrate is cleaved into OAA and acetyl-CoA which can be used for fatty acid (FA) biosynthesis. However, in the fungus Mucor circinelloides the molecular mechanism of citrate efflux from the mitochondria by this system and its role in FA synthesis is unclear. In the present study, we have analyzed the genome of high lipid-producing strain WJ11 and the low lipid-producing strain CBS 277.49 to find the potential genes involving in this system. Five potential genes are present in the genome of WJ11. These genes encode one citrate transport protein (CT), one tricarboxylate carrier (TCT), one MT, and two 2-oxoglutarate:malate antiporters (SoDIT-a and SoDIT-b). However, the genome of CBS 277.49 contains the same set of genes, except for the presence of just one SoDIT. The proteins from WJ11 had similar properties as their counterparts in CBS 277.49. Moreover, phylogenetic analyses revealed the evolutionary relationship of these proteins and illuminated their typical motifs related to potential functions. Additionally, the expression of these genes was analyzed to predict the possible functions in lipid metabolism in M. circinelloides. This is the first study to report the in silico analysis of structures and functions of the mitochondrial citrate transport system in M. circinelloides. This work showed a new strategy for research for the selection of candidate genes for further detailed functional investigation of the mitochondrial citrate transport system in lipid accumulation.

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Acknowledgements

We would like to thank Professor Wanwipa Vongsangnak in Computational Biomodelling Laboratory for Agricultural Science and Technology (CBLAST), Faculty of Science, Kasetsart University, Thailand, for computational facilities and Yao Zhang for data analysis work supported by the Key Research and Development Project of Shandong Province (2018GSF121013).

Funding

This work was supported by National Natural Science Foundation of China (Grant No. 31670064), TaiShan Industrial Experts Programme (tscy 20160101), the Key Research and Development Project of Shandong Province (2018GNC110039), Starting Grant from Shandong University of Technology and the Plan to Introduce High-Quality Foreign Experts in Zibo City.

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  1. Both Junhuan Yang and Md. Ahsanul Kabir Khan contributed equally to this work and are considered as first authors.

Authors and Affiliations

  1. Colin Ratledge Center for Microbial Lipids, School of Agricultural Engineering and Food Science, Shandong University of Technology, Zibo, 255000, Shandong, People’s Republic of China

    Junhuan Yang, Md. Ahsanul Kabir Khan, Huaiyuan Zhang, Yao Zhang & Yuanda Song

  2. Institute of Biotechnology, Faculty of Chemical and Food Technology, Slovak University of Technology, Radlinskeho 9, 812 37, Bratislava, Slovakia

    Milan Certik

  3. Departmento de Genética Y Microbiología (Unidad Asociada Al Instituto de Química Física Rocasolano, Consejo Superior de Investigaciones Científicas), Facultad de Biología, Universidad de Murcia, 30100, Murcia, Spain

    Victoriano Garre

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Contributions

Junhuan Yang and Md. Ahsanul Kabir Khan performed the experimental design, computational analysis, fermentation testing, manuscript writing, and figures and tables arrangement. Huaiyuan Zhang and Yao Zhang were involved in the experimental design. Victoriano Garre carried out results interpretation and reviewed of final draft. Yuanda Song proposed the project and was involved in data analysis, result interpretation, manuscript writing, and review of the final draft.

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284_2019_1822_MOESM1_ESM.docx

Supplementary file1 (DOCX 137 kb) S1. List of 51 candidates of mitochondrial transporter genes with predicted functions from TCDB. S2. Cell growth and lipid accumulation in M. circinelloides WJ11 and CBS 277.49. S3. Primers used in this study.

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Yang, J., Khan, M.A.K., Zhang, H. et al. Mitochondrial Citrate Transport System in the Fungus Mucor circinelloides: Identification, Phylogenetic Analysis, and Expression Profiling During Growth and Lipid Accumulation. Curr Microbiol 77, 220–231 (2020). https://doi.org/10.1007/s00284-019-01822-5

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