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

Jaeger, Daniel; Winkler, Anderson M.; Mussgnug, Jan H.; Kalinowski, Jörn; Goesmann, Alexander; Kruse, Olaf

doi:10.1186/s13068-017-0882-1

Cited by 38 publications

(27 citation statements)

References 152 publications

(292 reference statements)

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“…Firstly, ferredoxin NADP reductase (FNR), catalyzing the NADPH-producing step in photosynthesis, was up-regulated (Additional file 13: Data S11). This is interesting and different from the results under ND conditions where FNR gene was down-regulated in algae [15,56,90]. Secondly, the enzymes responsible for the two NADPH-producing steps in the oxidative pentose phosphate (OPP) pathway, glucose-6-phosphate dehydrogenase (G6PDH) and 6-phosphogluconate dehydrogenase (6PGD), were all upregulated at the transcriptional level (Additional file 13: Data S11), in agreement with the results under ND conditions [15].…”

Section: Stimulated Generation Of Reductant and Energysupporting

confidence: 57%

“…It is likely that upon salt treatment C. zofingiensis maintained the synthesis of membrane glycerolipids, but up-regulated the expression of lipases responsible for membrane lipid degradation, thereby stimulating the turnover towards decreased polar lipids. There are a number of putative membrane lipase-encoding genes found in algae and many were considerably up-regulated under TAG induction conditions [15,[55][56][57]. Among these lipases, PGD1 from C. reinhardtii has been well investigated and showed to play a role in MGDG degradation [52].…”

Section: Salt Stress Likely Stimulates the Turnover Of Membrane Lipidsmentioning

confidence: 99%

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Novel insights into salinity-induced lipogenesis and carotenogenesis in the oleaginous astaxanthin-producing alga Chromochloris zofingiensis: a multi-omics study

Mao

Zhang

Wang

et al. 2020

Biotechnol Biofuels

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Background: Chromochloris zofingiensis, a freshwater alga capable of synthesizing both triacylglycerol (TAG) and astaxanthin, has been receiving increasing attention as a leading candidate producer. While the mechanism of oleaginousness and/or carotenogenesis has been studied under such induction conditions as nitrogen deprivation, high light and glucose feeding, it remains to be elucidated in response to salt stress, a condition critical for reducing freshwater footprint during algal production processes. Results:Firstly, the effect of salt concentrations on growth, lipids and carotenoids was examined for C. zofingiensis, and 0.2 M NaCl demonstrated to be the optimal salt concentration for maximizing both TAG and astaxanthin production. Then, the time-resolved lipid and carotenoid profiles and comparative transcriptomes and metabolomes were generated in response to the optimized salt concentration for congruent analysis. A global response was triggered in C. zofingiensis allowing acclimation to salt stress, including photosynthesis impairment, ROS build-up, protein turnover, starch degradation, and TAG and astaxanthin accumulation. The lipid metabolism involved a set of stimulated biological pathways that contributed to carbon precursors, energy and reductant molecules, pushing and pulling power, and storage sink for TAG accumulation. On the other hand, salt stress suppressed lutein biosynthesis, stimulated astaxanthin biosynthesis (mainly via ketolation), yet had little effect on total carotenoid flux, leading to astaxanthin accumulation at the expense of lutein. Astaxanthin was predominantly esterified and accumulated in a well-coordinated manner with TAG, pointing to the presence of common regulators and potential communication for the two compounds. Furthermore, the comparison between salt stress and nitrogen deprivation conditions revealed distinctions in TAG and astaxanthin biosynthesis as well as critical genes with engineering potential. Conclusions:Our multi-omics data and integrated analysis shed light on the salt acclimation of C. zofingiensis and underlying mechanisms of TAG and astaxanthin biosynthesis, provide engineering implications into future trait improvements, and will benefit the development of this alga for production uses under saline environment, thus reducing the footprint of freshwater.

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Section: Stimulated Generation Of Reductant and Energysupporting

confidence: 57%

Section: Salt Stress Likely Stimulates the Turnover Of Membrane Lipidsmentioning

confidence: 99%

Novel insights into salinity-induced lipogenesis and carotenogenesis in the oleaginous astaxanthin-producing alga Chromochloris zofingiensis: a multi-omics study

Mao

Zhang

Wang

et al. 2020

Biotechnol Biofuels

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“…This may partially explain why C. zofingiensis is capable of synthesizing considerably larger amounts of TAG than C. reinhardtii under both NR and ND conditions. C. zofingiensis also had a considerable higher level of DGAT transcripts than M. neglectum , although they had a comparable number of DGAT genes (Jaeger et al ., ). Fifth, unique to C. zofingiensis , TAG and astaxanthin ester, which share common precursors, accumulate in a well coordinated way (Liu et al ., ).…”

Section: Resultsmentioning

confidence: 97%

“…For comparison, three other algae were employed including the model alga C. reinhardtii (Blaby et al ., ), the oleaginous green alga Monoraphidium neglectum (Jaeger et al ., ) and the oleaginous heterokont N. oceanica (Li et al ., ), which all had ND‐induced time‐resolved transcriptomes. The three green algae differed greatly from N. oceanica except for energy production, which was produced mainly by upregulating glycolysis and the TCA cycle (Table ).…”

Section: Resultsmentioning

confidence: 99%

Multiomics analysis reveals a distinct mechanism of oleaginousness in the emerging model alga Chromochloris zofingiensis

et al. 2019

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Chromochloris zofingiensis, featured due to its capability to simultaneously synthesize triacylglycerol (TAG) and astaxanthin, is emerging as a leading candidate alga for production uses. To better understand the oleaginous mechanism of this alga, we conducted a multiomics analysis by systematically integrating timeresolved transcriptomes, lipidomes and metabolomes in response to nitrogen deprivation. The data analysis unraveled the distinct mechanism of TAG accumulation, which involved coordinated stimulation of multiple biological processes including supply of energy and reductants, carbon reallocation from protein and starch, and 'pushing' and 'pulling' carbon to TAG synthesis. Unlike the model alga Chlamydomonas, de novo fatty acid synthesis in C. zofingiensis was promoted, together with enhanced turnover of both glycolipids and phospholipids, supporting the drastic need of acyls for TAG assembly. Moreover, genomewide analysis identified many key functional enzymes and transcription factors that had engineering potential for TAG modulation. Two genes encoding glycerol-3-phosphate acyltransferase (GPAT), the first committed enzyme for TAG assembly, were found in the C. zofingiensis genome; in vivo functional characterization revealed that extrachloroplastic GPAT instead of chloroplastic GPAT played a central role in TAG synthesis. These findings illuminate distinct oleaginousness mechanisms in C. zofingiensis and pave the way towards rational manipulation of this alga to becone an emerging model for trait improvements.

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“…cDNA library and illumina sequencing were performed as previously described (Jaeger et al, 2017b). For each timepoint three biological replicates were used and processed individually.…”

Section: Methodsmentioning

confidence: 99%

Ubiquitin ligase component LRS1 and transcription factor CrHy5 act as a light switch for photoprotection inChlamydomonas

Lämmermann

Wulf

Chang

et al. 2020

Preprint

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25Survival under excess light conditions requires the light-induced accumulation of protein 26 LHCSR3 and other photoprotection factors, to enable efficient energy-dependent 27 quenching in the green microalga Chlamydomonas reinhardtii. Here, we demonstrate 28 that the high light-tolerant phenotype of mutant hit1 is caused by a de-repression of 29 promoters belonging to photoprotection genes, which in turn results from an inactivation 30 of the E3 ubiquitin ligase substrate adaptor LRS1. Transcriptome analyses of hit1 31 revealed massive alterations of gene expression modulation as a consequence of 32 perturbed LRS1 function, indicating its role as a crown regulator. In conjunction with 33 random forest-based network modeling, these transcriptome analyses predicted that 34 LRS1 controls photoprotection gene expression via an algal HY5 homolog as its prime 35 transcription factor target. CrHY5 binds to T-box elements present in the promoters of 36 these genes and its inactivation in the hit1 mutant via CRISPR-Cas9 genome editing, 37 confirmed the regulatory connection between LRS1 and CrHY5, predicted by the 38 network analysis. 39 40 41 42 43 44 45 46 47 48 54 Light provides the energy driving photosynthesis and it is an important cue controlling 55 many physiological processes in phototrophic organisms. In the seed plant Arabidopsis 56 thaliana the E3 ubiquitin ligase substrate adaptor COP1/SPA is a master switch of light 57 signaling, by repressing the accumulation of various transcription factors required for the 58 induction of light-dependent processes like photomorphogenesis or flowering in 59 darkness. Repression is achieved by ubiquitination of target transcription factors and 60

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

Cited by 38 publications

References 152 publications

Novel insights into salinity-induced lipogenesis and carotenogenesis in the oleaginous astaxanthin-producing alga Chromochloris zofingiensis: a multi-omics study

Novel insights into salinity-induced lipogenesis and carotenogenesis in the oleaginous astaxanthin-producing alga Chromochloris zofingiensis: a multi-omics study

Multiomics analysis reveals a distinct mechanism of oleaginousness in the emerging model alga Chromochloris zofingiensis

Ubiquitin ligase component LRS1 and transcription factor CrHy5 act as a light switch for photoprotection inChlamydomonas

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