Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen Deprivation

HIGHLIGHTSAn electrospray ionization mass spectrometry-based lipidomics method was developed and integrated with transcriptomics to elucidate metabolic remodeling and turnover of microalgal membrane lipids by using Nannochloropsis oceanica as a model.The lack of lipidome analytical tools has limited...

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Main Authors: Danxiang Han, Jing Jia, Jing Li, Milton Sommerfeld, Jian Xu, Qiang Hu
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-08-01
Series:Frontiers in Marine Science
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fmars.2017.00242/full
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spelling doaj-9e7a0d47e8fc484d8efbbf0992df6b1a2020-11-24T23:24:37ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452017-08-01410.3389/fmars.2017.00242277428Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen DeprivationDanxiang Han0Jing Jia1Jing Jia2Jing Li3Milton Sommerfeld4Jian Xu5Qiang Hu6Qiang Hu7Qiang Hu8Center for Microalgal Biofuels and Biotechnology, Institute of Hydrobiology, Chinese Academy of SciencesWuhan, ChinaCenter for Microalgal Biofuels and Biotechnology, Institute of Hydrobiology, Chinese Academy of SciencesWuhan, ChinaSDIC Microalgae Biotechnology Center, China Electronics Engineering Design Institute, State Development and Investment CorporationBeijing, ChinaCAS Key Laboratory of Genome Sciences and Information, Beijing Institute of Genomics, Chinese Academy of SciencesBeijing, ChinaLaboratory for Algae Research and Biotechnology, Department of Applied Biological Sciences, Arizona State UniversityMesa, AZ, United StatesCAS Key Laboratory of Biofuels and Shandong Key Laboratory of Energy Genetics and BioEnergy Genome Center, Single-Cell Center, Qingdao Institute of BioEnergy and Bioprocess Technology, Chinese Academy of SciencesQingdao, ChinaCenter for Microalgal Biofuels and Biotechnology, Institute of Hydrobiology, Chinese Academy of SciencesWuhan, ChinaSDIC Microalgae Biotechnology Center, China Electronics Engineering Design Institute, State Development and Investment CorporationBeijing, ChinaKey Laboratory of Algal Biology, Institute of Hydrobiology, Chinese Academy of SciencesWuhan, ChinaHIGHLIGHTSAn electrospray ionization mass spectrometry-based lipidomics method was developed and integrated with transcriptomics to elucidate metabolic remodeling and turnover of microalgal membrane lipids by using Nannochloropsis oceanica as a model.The lack of lipidome analytical tools has limited our ability to gain new knowledge about lipid metabolism in microalgae, especially for membrane glycerolipids. An electrospray ionization mass spectrometry-based lipidomics method was developed for Nannochloropsis oceanica IMET1, which resolved 41 membrane glycerolipids molecular species belonging to eight classes. Changes in membrane glycerolipids under nitrogen deprivation and high-light (HL) conditions were uncovered. The results showed that the amount of plastidial membrane lipids including monogalactosyldiacylglycerol, phosphatidylglycerol, and the extraplastidic lipids diacylglyceryl-O-4′-(N, N, N,-trimethyl) homoserine and phosphatidylcholine decreased drastically under HL and nitrogen deprivation stresses. Algal cells accumulated considerably more digalactosyldiacylglycerol and sulfoquinovosyldiacylglycerols under stresses. The genes encoding enzymes responsible for biosynthesis, modification and degradation of glycerolipids were identified by mining a time-course global RNA-seq data set. It suggested that reduction in lipid contents under nitrogen deprivation is not attributable to the retarded biosynthesis processes, at least at the gene expression level, as most genes involved in their biosynthesis were unaffected by nitrogen supply, yet several genes were significantly up-regulated. Additionally, a conceptual eicosapentaenoic acid (EPA) biosynthesis network is proposed based on the lipidomic and transcriptomic data, which underlined import of EPA from cytosolic glycerolipids to the plastid for synthesizing EPA-containing chloroplast membrane lipids.http://journal.frontiersin.org/article/10.3389/fmars.2017.00242/fullNannochloropsis oceanicamembrane glycerolipidlipidomicstranscriptomicsenvironmental stresseseicosapentaenoic acid
collection DOAJ
language English
format Article
sources DOAJ
author Danxiang Han
Jing Jia
Jing Jia
Jing Li
Milton Sommerfeld
Jian Xu
Qiang Hu
Qiang Hu
Qiang Hu
spellingShingle Danxiang Han
Jing Jia
Jing Jia
Jing Li
Milton Sommerfeld
Jian Xu
Qiang Hu
Qiang Hu
Qiang Hu
Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen Deprivation
Frontiers in Marine Science
Nannochloropsis oceanica
membrane glycerolipid
lipidomics
transcriptomics
environmental stresses
eicosapentaenoic acid
author_facet Danxiang Han
Jing Jia
Jing Jia
Jing Li
Milton Sommerfeld
Jian Xu
Qiang Hu
Qiang Hu
Qiang Hu
author_sort Danxiang Han
title Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen Deprivation
title_short Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen Deprivation
title_full Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen Deprivation
title_fullStr Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen Deprivation
title_full_unstemmed Metabolic Remodeling of Membrane Glycerolipids in the Microalga Nannochloropsis oceanica under Nitrogen Deprivation
title_sort metabolic remodeling of membrane glycerolipids in the microalga nannochloropsis oceanica under nitrogen deprivation
publisher Frontiers Media S.A.
series Frontiers in Marine Science
issn 2296-7745
publishDate 2017-08-01
description HIGHLIGHTSAn electrospray ionization mass spectrometry-based lipidomics method was developed and integrated with transcriptomics to elucidate metabolic remodeling and turnover of microalgal membrane lipids by using Nannochloropsis oceanica as a model.The lack of lipidome analytical tools has limited our ability to gain new knowledge about lipid metabolism in microalgae, especially for membrane glycerolipids. An electrospray ionization mass spectrometry-based lipidomics method was developed for Nannochloropsis oceanica IMET1, which resolved 41 membrane glycerolipids molecular species belonging to eight classes. Changes in membrane glycerolipids under nitrogen deprivation and high-light (HL) conditions were uncovered. The results showed that the amount of plastidial membrane lipids including monogalactosyldiacylglycerol, phosphatidylglycerol, and the extraplastidic lipids diacylglyceryl-O-4′-(N, N, N,-trimethyl) homoserine and phosphatidylcholine decreased drastically under HL and nitrogen deprivation stresses. Algal cells accumulated considerably more digalactosyldiacylglycerol and sulfoquinovosyldiacylglycerols under stresses. The genes encoding enzymes responsible for biosynthesis, modification and degradation of glycerolipids were identified by mining a time-course global RNA-seq data set. It suggested that reduction in lipid contents under nitrogen deprivation is not attributable to the retarded biosynthesis processes, at least at the gene expression level, as most genes involved in their biosynthesis were unaffected by nitrogen supply, yet several genes were significantly up-regulated. Additionally, a conceptual eicosapentaenoic acid (EPA) biosynthesis network is proposed based on the lipidomic and transcriptomic data, which underlined import of EPA from cytosolic glycerolipids to the plastid for synthesizing EPA-containing chloroplast membrane lipids.
topic Nannochloropsis oceanica
membrane glycerolipid
lipidomics
transcriptomics
environmental stresses
eicosapentaenoic acid
url http://journal.frontiersin.org/article/10.3389/fmars.2017.00242/full
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