Dataset Information

Elevated pCO2 Level Affects the Extracellular Polymer Metabolism of Phaeodactylum tricornutum.

ABSTRACT: Extracellular polymeric substances (EPS) play an important role in diatom physiology and carbon biogeochemical cycling in marine ecosystems. Both the composition and yield of EPS in diatom cells can vary with environmental changes. However, information on intracellular pathways and controls of both biochemical and genetic of EPS is limited. Further, how such changes would affect their critical ecological roles in marine systems is also unclear. Here, we evaluated the physiological characteristics, EPS yields, EPS compositions, and gene expression levels of Phaeodactylum tricornutum under elevated pCO2 levels. Genes and pathways related to EPS metabolism in P. tricornutum were identified. Carbohydrate yields in different EPS fractions increased with elevated pCO2 exposure. Although the proportions of monosaccharide sugars among total sugars did not change, higher abundances of uronic acid were observed under high pCO2 conditions, suggesting the alterations of EPS composition. Elevated pCO2 increased PSII light energy conversion efficiency and carbon sequestration efficiency. The up-regulation of most genes involved in carbon fixation pathways led to increased growth and EPS release. RNA-Seq analysis revealed a number of genes and divergent alleles related to EPS production that were up-regulated by elevated pCO2 levels. Nucleotide diphosphate (NDP)-sugar activation and accelerated glycosylation could be responsible for more EPS responding to environmental signals. Further, NDP-sugar transporters exhibited increased expression levels, suggesting roles in EPS over-production. Overall, these results provide critical data for understanding the mechanisms of EPS production in diatoms and evaluating the metabolic plasticity of these organisms in response to environmental changes.

SUBMITTER: Zhang W

PROVIDER: S-EPMC7064563 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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Elevated pCO2 Level Affects the Extracellular Polymer Metabolism of Phaeodactylum tricornutum.

Zhang Wei W Tang Xuexi X Yang Yingying Y Zhang Xin X Zhang Xinxin X

Frontiers in microbiology 20200304

Extracellular polymeric substances (EPS) play an important role in diatom physiology and carbon biogeochemical cycling in marine ecosystems. Both the composition and yield of EPS in diatom cells can vary with environmental changes. However, information on intracellular pathways and controls of both biochemical and genetic of EPS is limited. Further, how such changes would affect their critical ecological roles in marine systems is also unclear. Here, we evaluated the physiological characteristic ...[more]

PMID: 32194534

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Project description:BackgroundNumerous studies have shown that stress induction and genetic engineering can effectively increase lipid accumulation, but lead to a decrease of growth in the majority of microalgae. We previously found that elevated CO2 concentration increased lipid productivity as well as growth in Phaeodactylum tricornutum, along with an enhancement of the oxidative pentose phosphate pathway (OPPP) activity. The purpose of this work directed toward the verification of the critical role of glucose-6-phosphate dehydrogenase (G6PDH), the rate-limiting enzyme in the OPPP, in lipid accumulation in P. tricornutum and its simultaneous rapid growth rate under high-CO2 (0.15%) cultivation.ResultsIn this study, G6PDH was identified as a target for algal strain improvement, wherein G6PDH gene was successfully overexpressed and antisense knockdown in P. tricornutum, and systematic comparisons of the photosynthesis performance, algal growth, lipid content, fatty acid profiles, NADPH production, G6PDH activity and transcriptional abundance were performed. The results showed that, due to the enhanced G6PDH activity, transcriptional abundance and NAPDH production, overexpression of G6PDH accompanied by high-CO2 cultivation resulted in a much higher of both lipid content and growth in P. tricornutum, while knockdown of G6PDH greatly decreased algal growth as well as lipid accumulation. In addition, the total proportions of saturated and unsaturated fatty acid, especially the polyunsaturated fatty acid eicosapentaenoic acid (EPA; C20:5, n-3), were highly increased in high-CO2 cultivated G6PDH overexpressed strains.ConclusionsThe successful of overexpression and antisense knockdown of G6PDH well demonstrated the positive influence of G6PDH on algal growth and lipid accumulation in P. tricornutum. The improvement of algal growth, lipid content as well as polyunsaturated fatty acids in high-CO2 cultivated G6PDH overexpressed P. tricornutum suggested this G6PDH overexpression-high CO2 cultivation pattern provides an efficient and economical route for algal strain improvement to develop algal-based biodiesel production.

Project description:BackgroundHeterotrophic fermentation using simple sugars such as glucose is an established and cost-effective method for synthesizing bioproducts from bacteria, yeast and algae. Organisms incapable of metabolizing glucose have limited applications as cell factories, often despite many other advantageous characteristics. Therefore, there is a clear need to investigate glucose metabolism in potential cell factories. One such organism, with a unique metabolic network and a propensity to synthesize highly reduced compounds as a large fraction of its biomass, is the marine diatom Phaeodactylum tricornutum (Pt). Although Pt has been engineered to metabolize glucose, conflicting lines of evidence leave it unresolved whether Pt can natively consume glucose.ResultsIsotope labeling experiments in which Pt was mixotrophically grown under light on 100% U-(13)C glucose and naturally abundant (~99% (12)C) dissolved inorganic carbon resulted in proteinogenic amino acids with an average 13C-enrichment of 88%, thus providing convincing evidence of glucose uptake and metabolism. The dissolved inorganic carbon was largely incorporated through anaplerotic rather than photosynthetic fixation. Furthermore, an isotope labeling experiment utilizing 1-(13)C glucose and subsequent metabolic pathway analysis indicated that (i) the alternative Entner-Doudoroff and Phosphoketolase glycolytic pathways are active during glucose metabolism, and (ii) during mixotrophic growth, serine and glycine are largely synthesized from glyoxylate through photorespiratory reactions rather than from 3-phosphoglycerate. We validated the latter result for mixotrophic growth on glycerol by performing a 2-(13)C glycerol isotope labeling experiment. Additionally, gene expression assays showed that known, native glucose transporters in Pt are largely insensitive to glucose or light, whereas the gene encoding cytosolic fructose bisphosphate aldolase 3, an important glycolytic enzyme, is overexpressed in light but insensitive to glucose.ConclusionWe have shown that Pt can use glucose as a primary carbon source when grown in light, but cannot use glucose to sustain growth in the dark. We further analyzed the metabolic mechanisms underlying the mixotrophic metabolism of glucose and found isotopic evidence for unusual pathways active in Pt. These insights expand the envelope of Pt cultivation methods using organic substrates. We anticipate that they will guide further engineering of Pt towards sustainable production of fuels, pharmaceuticals, and platform chemicals.

Dataset Information

Elevated pCO2 Level Affects the Extracellular Polymer Metabolism of Phaeodactylum tricornutum.

Publications

Elevated <i>p</i>CO<sub>2</sub> Level Affects the Extracellular Polymer Metabolism of <i>Phaeodactylum tricornutum</i>.

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