Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation

Abstract Background Oleaginous microalgae are promising production hosts for the sustainable generation of lipid-based bioproducts and as bioenergy carriers such as biodiesel. Transcriptomics of the lipid accumulation phase, triggered efficiently by nitrogen starvation, is a valuable approach for th...

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Main Authors: Daniel Jaeger, Anika Winkler, Jan H. Mussgnug, Jörn Kalinowski, Alexander Goesmann, Olaf Kruse
Format: Article
Language:English
Published: BMC 2017-08-01
Series:Biotechnology for Biofuels
Subjects:
Online Access:http://link.springer.com/article/10.1186/s13068-017-0882-1
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author Daniel Jaeger
Anika Winkler
Jan H. Mussgnug
Jörn Kalinowski
Alexander Goesmann
Olaf Kruse
author_facet Daniel Jaeger
Anika Winkler
Jan H. Mussgnug
Jörn Kalinowski
Alexander Goesmann
Olaf Kruse
author_sort Daniel Jaeger
collection DOAJ
description Abstract Background Oleaginous microalgae are promising production hosts for the sustainable generation of lipid-based bioproducts and as bioenergy carriers such as biodiesel. Transcriptomics of the lipid accumulation phase, triggered efficiently by nitrogen starvation, is a valuable approach for the identification of gene targets for metabolic engineering. Results An explorative analysis of the detailed transcriptional response to different stages of nitrogen availability was performed in the oleaginous green alga Monoraphidium neglectum. Transcript data were correlated with metabolic data for cellular contents of starch and of different lipid fractions. A pronounced transcriptional down-regulation of photosynthesis became apparent in response to nitrogen starvation, whereas glucose catabolism was found to be up-regulated. An in-depth reconstruction and analysis of the pathways for glycerolipid, central carbon, and starch metabolism revealed that distinct transcriptional changes were generally found only for specific steps within a metabolic pathway. In addition to pathway analyses, the transcript data were also used to refine the current genome annotation. The transcriptome data were integrated into a database and complemented with data for other microalgae which were also subjected to nitrogen starvation. It is available at https://tdbmn.cebitec.uni-bielefeld.de . Conclusions Based on the transcriptional responses to different stages of nitrogen availability, a model for triacylglycerol and lipid hyperaccumulation is proposed, which involves transcriptional induction of thioesterases, differential regulation of lipases, and a re-routing of the central carbon metabolism. Over-expression of distinct thioesterases was identified to be a potential strategy to increase the oleaginous phenotype of M. neglectum, and furthermore specific lipases were identified as potential targets for future metabolic engineering approaches.
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spelling doaj.art-f7888deafe3f446495b99035722124c52022-12-22T03:35:26ZengBMCBiotechnology for Biofuels1754-68342017-08-0110113410.1186/s13068-017-0882-1Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulationDaniel Jaeger0Anika Winkler1Jan H. Mussgnug2Jörn Kalinowski3Alexander Goesmann4Olaf Kruse5Algae Biotechnology and Bioenergy, Faculty of Biology, Center for Biotechnology (CeBiTec), Bielefeld UniversityMicrobial Genomics and Biotechnology, Center for Biotechnology (CeBiTec), Bielefeld UniversityAlgae Biotechnology and Bioenergy, Faculty of Biology, Center for Biotechnology (CeBiTec), Bielefeld UniversityMicrobial Genomics and Biotechnology, Center for Biotechnology (CeBiTec), Bielefeld UniversityBioinformatics and Systems Biology, Justus-Liebig-UniversitätAlgae Biotechnology and Bioenergy, Faculty of Biology, Center for Biotechnology (CeBiTec), Bielefeld UniversityAbstract Background Oleaginous microalgae are promising production hosts for the sustainable generation of lipid-based bioproducts and as bioenergy carriers such as biodiesel. Transcriptomics of the lipid accumulation phase, triggered efficiently by nitrogen starvation, is a valuable approach for the identification of gene targets for metabolic engineering. Results An explorative analysis of the detailed transcriptional response to different stages of nitrogen availability was performed in the oleaginous green alga Monoraphidium neglectum. Transcript data were correlated with metabolic data for cellular contents of starch and of different lipid fractions. A pronounced transcriptional down-regulation of photosynthesis became apparent in response to nitrogen starvation, whereas glucose catabolism was found to be up-regulated. An in-depth reconstruction and analysis of the pathways for glycerolipid, central carbon, and starch metabolism revealed that distinct transcriptional changes were generally found only for specific steps within a metabolic pathway. In addition to pathway analyses, the transcript data were also used to refine the current genome annotation. The transcriptome data were integrated into a database and complemented with data for other microalgae which were also subjected to nitrogen starvation. It is available at https://tdbmn.cebitec.uni-bielefeld.de . Conclusions Based on the transcriptional responses to different stages of nitrogen availability, a model for triacylglycerol and lipid hyperaccumulation is proposed, which involves transcriptional induction of thioesterases, differential regulation of lipases, and a re-routing of the central carbon metabolism. Over-expression of distinct thioesterases was identified to be a potential strategy to increase the oleaginous phenotype of M. neglectum, and furthermore specific lipases were identified as potential targets for future metabolic engineering approaches.http://link.springer.com/article/10.1186/s13068-017-0882-1Monoraphidium neglectummRNA-seqBiodieselLipid metabolismNitrogen starvationTAG accumulation
spellingShingle Daniel Jaeger
Anika Winkler
Jan H. Mussgnug
Jörn Kalinowski
Alexander Goesmann
Olaf Kruse
Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation
Biotechnology for Biofuels
Monoraphidium neglectum
mRNA-seq
Biodiesel
Lipid metabolism
Nitrogen starvation
TAG accumulation
title Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation
title_full Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation
title_fullStr Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation
title_full_unstemmed Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation
title_short Time-resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga Monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation
title_sort time resolved transcriptome analysis and lipid pathway reconstruction of the oleaginous green microalga monoraphidium neglectum reveal a model for triacylglycerol and lipid hyperaccumulation
topic Monoraphidium neglectum
mRNA-seq
Biodiesel
Lipid metabolism
Nitrogen starvation
TAG accumulation
url http://link.springer.com/article/10.1186/s13068-017-0882-1
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