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Lipid droplets accumulation and other biochemical changes induced in the fungal pathogen Ustilago maydis under nitrogen-starvation

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Abstract

In many organisms, the growth under nitrogen-deprivation or a poor nitrogen source impacts on the carbon flow distribution and causes accumulation of neutral lipids, which are stored as lipid droplets (LDs). Efforts are in progress to find the mechanism of LDs synthesis and degradation, and new organisms capable of accumulating large amounts of lipids for biotechnological applications. In this context, when Ustilago maydis was cultured in the absence of a nitrogen source, there was a large accumulation of lipid bodies containing mainly triacylglycerols. The most abundant fatty acids in lipid bodies at the stationary phase were palmitic, linoleic, and oleic acids, and they were synthesized de novo by the fatty-acid synthase. In regard to the production of NADPH for the synthesis of fatty acids, the cytosolic NADP+-dependent isocitrate dehydrogenase and the glucose-6-phosphate and 6-phosphogluconate dehydrogenases couple showed the highest specific activities, with a lower activity of the malic enzyme. The ATP-citrate lyase activity was not detected in any of the culture conditions, which points to a different mechanism for the transfer of acetyl-CoA into the cytosol. Protein and RNA contents decreased when U. maydis was grown without a nitrogen source. Due to the significant accumulation of triacylglycerols and the particular composition of fatty acids, U. maydis can be considered an alternative model for biotechnological applications.

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Acknowledgements

This work is part of Ph.D. studies of Lucero Romero Aguilar, who received scholarship from CONACYT-México (237219). This work was supported by grants IPN-SIP-20141521, 20150761, and 20160999, Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT IN222117), Universidad Nacional Autónoma de México (UNAM), and Consejo Nacional de Ciencia y Tecnología (CONACyT 254904-JPP and 256520-GGS). Fundação de Amparo a Pesquisa do Rio de Janeiro (FAPERJ-Cientistas do Nosso Estado: E 26/103.353/2011). We thank Prof. Miguel Tapia Rodríguez for the advice with the Confocal Microscopy, and Rodolfo Paredes Díaz for the technical support with the Transmission Electron Microscopy. We also thank Juliana Bernardo Madeira from UFRJ-Brazil for her advice to develop the LRF assay in Ustilago maydis. Authors want to thank Mrs. Josefina Bolado, Head of the Scientific Paper Translation Department, from División de Investigación at Facultad de Medicina, UNAM, for editing the English-language version of this manuscript.

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Contributions

LRA performed experiments, analyzed data, planned experiments, and participated in the writing of the manuscript. JPP and GGSplanned experiments, analyzed data, and participated in the writing of the manuscript. MAJO and OILB performed the GC–MS and lipid neutral analysis. MML planned experiments and contributed with reagents and equipment.

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Correspondence to Juan Pablo Pardo or Guadalupe Guerra Sánchez.

Additional information

Communicated by Erko Stackebrandt.

Guadalupe Guerra Sánchez and Juan Pablo Pardo share the senior co-authorship as corresponding authors.

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Aguilar, L.R., Pardo, J.P., Lomelí, M.M. et al. Lipid droplets accumulation and other biochemical changes induced in the fungal pathogen Ustilago maydis under nitrogen-starvation. Arch Microbiol 199, 1195–1209 (2017). https://doi.org/10.1007/s00203-017-1388-8

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  • DOI: https://doi.org/10.1007/s00203-017-1388-8

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