Orchestration of transcriptome, proteome and metabolome in the diatom Phaeodactylum tricornutum during nitrogen limitation

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Abstract

Nitrogen deprivation increases the triacylglycerol (TAG) content in microalgae but also severely decreases the growth rate. Most approaches that attempted to increase TAG productivity by overexpression or knockdown of specific genes related to the regulation of the lipid synthesis have reported only little success. More insight into the molecular mechanisms related to lipid accumulation and impaired growth rate is needed to find targets for improving TAG productivity. By using the emerging “omics” approach, we comprehensively profiled the physiology, transcriptome, proteome and metabolome of the diatom Phaeodactylum tricornutum during steady state growth at both nitrogen limited and replete levels during light:dark cycles. Under nitrogen limited conditions, 22% (2699) of the total identified transcripts, 17% (543) of the proteins and 44% (345) of the metabolites were significantly differentially regulated compared to nitrogen replete growth conditions. Although nitrogen limitation was responsible for the majority of significant differential transcript, protein and metabolite accumulation, we also observed differential expression over a diurnal cycle. Nitrogen limitation mainly induced an upregulation of nitrogen fixation, central carbon metabolism and TCA cycle, while photosynthetic and ribosomal protein synthesis are mainly downregulated. Regulation of the lipid metabolism and the expression of predicted proteins involved in lipid processes suggest that lipid rearrangements may substantially contribute to TAG distribution. However, TAG synthesis is also limited by the reduced carbon flux through central metabolism. Future strain improvements should therefore focus on understanding and improving the carbon flux through central carbon metabolism, selectivity and activity of DGAT isoforms and lipase enzymes.

LanguageEnglish
Pages33-49
JournalAlgal Research
Volume35
DOIs
Publication statusPublished - Nov 2018

Fingerprint

metabolome
Phaeodactylum tricornutum
Bacillariophyceae
proteome
transcriptome
triacylglycerols
nitrogen
carbon
lipids
metabolism
metabolites
synthesis
proteins
tricarboxylic acid cycle
ribosomal proteins
microalgae
nitrogen fixation
lipid metabolism
physiology
photoperiod

Keywords

  • Diatoms
  • Diurnal metabolism
  • Lipids
  • Mitochondrion
  • Omics
  • Triacylglycerol

Cite this

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title = "Orchestration of transcriptome, proteome and metabolome in the diatom Phaeodactylum tricornutum during nitrogen limitation",
abstract = "Nitrogen deprivation increases the triacylglycerol (TAG) content in microalgae but also severely decreases the growth rate. Most approaches that attempted to increase TAG productivity by overexpression or knockdown of specific genes related to the regulation of the lipid synthesis have reported only little success. More insight into the molecular mechanisms related to lipid accumulation and impaired growth rate is needed to find targets for improving TAG productivity. By using the emerging “omics” approach, we comprehensively profiled the physiology, transcriptome, proteome and metabolome of the diatom Phaeodactylum tricornutum during steady state growth at both nitrogen limited and replete levels during light:dark cycles. Under nitrogen limited conditions, 22{\%} (2699) of the total identified transcripts, 17{\%} (543) of the proteins and 44{\%} (345) of the metabolites were significantly differentially regulated compared to nitrogen replete growth conditions. Although nitrogen limitation was responsible for the majority of significant differential transcript, protein and metabolite accumulation, we also observed differential expression over a diurnal cycle. Nitrogen limitation mainly induced an upregulation of nitrogen fixation, central carbon metabolism and TCA cycle, while photosynthetic and ribosomal protein synthesis are mainly downregulated. Regulation of the lipid metabolism and the expression of predicted proteins involved in lipid processes suggest that lipid rearrangements may substantially contribute to TAG distribution. However, TAG synthesis is also limited by the reduced carbon flux through central metabolism. Future strain improvements should therefore focus on understanding and improving the carbon flux through central carbon metabolism, selectivity and activity of DGAT isoforms and lipase enzymes.",
keywords = "Diatoms, Diurnal metabolism, Lipids, Mitochondrion, Omics, Triacylglycerol",
author = "Remmers, {Ilse M.} and Sarah D'Adamo and Martens, {Dirk E.} and {de Vos}, {Ric C.H.} and Roland Mumm and America, {Antoine H.P.} and Cordewener, {Jan H.G.} and Bakker, {Linda V.} and Peters, {Sander A.} and Wijffels, {Ren{\'e} H.} and Lamers, {Packo P.}",
year = "2018",
month = "11",
doi = "10.1016/j.algal.2018.08.012",
language = "English",
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journal = "Algal Research",
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T1 - Orchestration of transcriptome, proteome and metabolome in the diatom Phaeodactylum tricornutum during nitrogen limitation

AU - Remmers, Ilse M.

AU - D'Adamo, Sarah

AU - Martens, Dirk E.

AU - de Vos, Ric C.H.

AU - Mumm, Roland

AU - America, Antoine H.P.

AU - Cordewener, Jan H.G.

AU - Bakker, Linda V.

AU - Peters, Sander A.

AU - Wijffels, René H.

AU - Lamers, Packo P.

PY - 2018/11

Y1 - 2018/11

N2 - Nitrogen deprivation increases the triacylglycerol (TAG) content in microalgae but also severely decreases the growth rate. Most approaches that attempted to increase TAG productivity by overexpression or knockdown of specific genes related to the regulation of the lipid synthesis have reported only little success. More insight into the molecular mechanisms related to lipid accumulation and impaired growth rate is needed to find targets for improving TAG productivity. By using the emerging “omics” approach, we comprehensively profiled the physiology, transcriptome, proteome and metabolome of the diatom Phaeodactylum tricornutum during steady state growth at both nitrogen limited and replete levels during light:dark cycles. Under nitrogen limited conditions, 22% (2699) of the total identified transcripts, 17% (543) of the proteins and 44% (345) of the metabolites were significantly differentially regulated compared to nitrogen replete growth conditions. Although nitrogen limitation was responsible for the majority of significant differential transcript, protein and metabolite accumulation, we also observed differential expression over a diurnal cycle. Nitrogen limitation mainly induced an upregulation of nitrogen fixation, central carbon metabolism and TCA cycle, while photosynthetic and ribosomal protein synthesis are mainly downregulated. Regulation of the lipid metabolism and the expression of predicted proteins involved in lipid processes suggest that lipid rearrangements may substantially contribute to TAG distribution. However, TAG synthesis is also limited by the reduced carbon flux through central metabolism. Future strain improvements should therefore focus on understanding and improving the carbon flux through central carbon metabolism, selectivity and activity of DGAT isoforms and lipase enzymes.

AB - Nitrogen deprivation increases the triacylglycerol (TAG) content in microalgae but also severely decreases the growth rate. Most approaches that attempted to increase TAG productivity by overexpression or knockdown of specific genes related to the regulation of the lipid synthesis have reported only little success. More insight into the molecular mechanisms related to lipid accumulation and impaired growth rate is needed to find targets for improving TAG productivity. By using the emerging “omics” approach, we comprehensively profiled the physiology, transcriptome, proteome and metabolome of the diatom Phaeodactylum tricornutum during steady state growth at both nitrogen limited and replete levels during light:dark cycles. Under nitrogen limited conditions, 22% (2699) of the total identified transcripts, 17% (543) of the proteins and 44% (345) of the metabolites were significantly differentially regulated compared to nitrogen replete growth conditions. Although nitrogen limitation was responsible for the majority of significant differential transcript, protein and metabolite accumulation, we also observed differential expression over a diurnal cycle. Nitrogen limitation mainly induced an upregulation of nitrogen fixation, central carbon metabolism and TCA cycle, while photosynthetic and ribosomal protein synthesis are mainly downregulated. Regulation of the lipid metabolism and the expression of predicted proteins involved in lipid processes suggest that lipid rearrangements may substantially contribute to TAG distribution. However, TAG synthesis is also limited by the reduced carbon flux through central metabolism. Future strain improvements should therefore focus on understanding and improving the carbon flux through central carbon metabolism, selectivity and activity of DGAT isoforms and lipase enzymes.

KW - Diatoms

KW - Diurnal metabolism

KW - Lipids

KW - Mitochondrion

KW - Omics

KW - Triacylglycerol

U2 - 10.1016/j.algal.2018.08.012

DO - 10.1016/j.algal.2018.08.012

M3 - Article

VL - 35

SP - 33

EP - 49

JO - Algal Research

T2 - Algal Research

JF - Algal Research

SN - 2211-9264

ER -