Physiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitions

Abstract Background Light is a key regulatory factor for photosynthesis and metabolism of microalgae. The diatom Phaeodactylum tricornutum is capable of exhibiting metabolic flexibility in response to light fluctuations. However, the metabolic switching and underlying molecular mechanisms upon illum...

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Main Authors: Wei Ding, Ying Ye, Lihua Yu, Meijing Liu, Jin Liu
Format: Article
Language:English
Published: BMC 2023-06-01
Series:Biotechnology for Biofuels and Bioproducts
Subjects:
Online Access:https://doi.org/10.1186/s13068-023-02352-w
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author Wei Ding
Ying Ye
Lihua Yu
Meijing Liu
Jin Liu
author_facet Wei Ding
Ying Ye
Lihua Yu
Meijing Liu
Jin Liu
author_sort Wei Ding
collection DOAJ
description Abstract Background Light is a key regulatory factor for photosynthesis and metabolism of microalgae. The diatom Phaeodactylum tricornutum is capable of exhibiting metabolic flexibility in response to light fluctuations. However, the metabolic switching and underlying molecular mechanisms upon illumination transitions remain poorly understood for this industrially relevant marine alga. To address these, the physiochemical and molecular responses of P. tricornutum upon high light (HL) and recovery (HLR) were probed. Results Upon HL, P. tricornutum exhibited quick responses, including decreases in cell division, major light harvesting pigments (e.g., chlorophyll a, β-carotene, and fucoxanthin), chloroplastidic membrane lipids (e.g., monogalactosyldiacylglycerol, digalactosyldiacylglycerol, and sulfoquinovosyldiacylglycerol), and long-chain polyunsaturated fatty acids (e.g., C20:5), as well as increases in carbohydrates and neutral lipids particularly triacylglycerol. During HLR stage when the stress was removed, these physiochemical phenotypes were generally recovered, indicative of a rapid and reversible changes of P. tricornutum to cope with illumination transitions for survival and growth. Through the integrated analysis with time-resolved transcriptomics, we revealed the transcriptional control of photosynthesis and carbon metabolism in P. tricornutum responding to HL, which could be reversed more or less during the HLR stage. Furthermore, we highlighted key enzymes involved in carotenoid biosynthesis and lipid metabolism of P. tricornutum and identified monooxygenases putatively responsible for catalyzing the ketolation step towards fucoxanthin synthesis from neoxanthin. Conclusions The detailed profiling of physiochemical and transcriptional responses of P. tricornutum to HL-HLR treatments advances our understanding on the adaption of the alga to illumination transitions and provides new insights into engineering of the alga for improved production of value-added carotenoids and lipids.
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spelling doaj.art-bd10a0e9be584ccf9906ea2fb7998b932023-06-18T11:09:08ZengBMCBiotechnology for Biofuels and Bioproducts2731-36542023-06-0116112210.1186/s13068-023-02352-wPhysiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitionsWei Ding0Ying Ye1Lihua Yu2Meijing Liu3Jin Liu4Laboratory for Algae Biotechnology & Innovation, College of Engineering, Peking UniversityLaboratory for Algae Biotechnology & Innovation, College of Engineering, Peking UniversityLaboratory for Algae Biotechnology & Innovation, College of Engineering, Peking UniversityLaboratory for Algae Biotechnology & Innovation, College of Engineering, Peking UniversityLaboratory for Algae Biotechnology & Innovation, College of Engineering, Peking UniversityAbstract Background Light is a key regulatory factor for photosynthesis and metabolism of microalgae. The diatom Phaeodactylum tricornutum is capable of exhibiting metabolic flexibility in response to light fluctuations. However, the metabolic switching and underlying molecular mechanisms upon illumination transitions remain poorly understood for this industrially relevant marine alga. To address these, the physiochemical and molecular responses of P. tricornutum upon high light (HL) and recovery (HLR) were probed. Results Upon HL, P. tricornutum exhibited quick responses, including decreases in cell division, major light harvesting pigments (e.g., chlorophyll a, β-carotene, and fucoxanthin), chloroplastidic membrane lipids (e.g., monogalactosyldiacylglycerol, digalactosyldiacylglycerol, and sulfoquinovosyldiacylglycerol), and long-chain polyunsaturated fatty acids (e.g., C20:5), as well as increases in carbohydrates and neutral lipids particularly triacylglycerol. During HLR stage when the stress was removed, these physiochemical phenotypes were generally recovered, indicative of a rapid and reversible changes of P. tricornutum to cope with illumination transitions for survival and growth. Through the integrated analysis with time-resolved transcriptomics, we revealed the transcriptional control of photosynthesis and carbon metabolism in P. tricornutum responding to HL, which could be reversed more or less during the HLR stage. Furthermore, we highlighted key enzymes involved in carotenoid biosynthesis and lipid metabolism of P. tricornutum and identified monooxygenases putatively responsible for catalyzing the ketolation step towards fucoxanthin synthesis from neoxanthin. Conclusions The detailed profiling of physiochemical and transcriptional responses of P. tricornutum to HL-HLR treatments advances our understanding on the adaption of the alga to illumination transitions and provides new insights into engineering of the alga for improved production of value-added carotenoids and lipids.https://doi.org/10.1186/s13068-023-02352-wIllumination transitionsCarbon metabolism reorientationPhotosynthesisPigmentsLipidsTranscriptomics
spellingShingle Wei Ding
Ying Ye
Lihua Yu
Meijing Liu
Jin Liu
Physiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitions
Biotechnology for Biofuels and Bioproducts
Illumination transitions
Carbon metabolism reorientation
Photosynthesis
Pigments
Lipids
Transcriptomics
title Physiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitions
title_full Physiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitions
title_fullStr Physiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitions
title_full_unstemmed Physiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitions
title_short Physiochemical and molecular responses of the diatom Phaeodactylum tricornutum to illumination transitions
title_sort physiochemical and molecular responses of the diatom phaeodactylum tricornutum to illumination transitions
topic Illumination transitions
Carbon metabolism reorientation
Photosynthesis
Pigments
Lipids
Transcriptomics
url https://doi.org/10.1186/s13068-023-02352-w
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