Non-Enzymatic Synthesis of Bioactive Isoprostanoids in the Diatom <i>Phaeodactylum</i> following Oxidative Stress

Lupette, Josselin; Jaussaud, Antoine; Vigor, Claire; Oger, Camille; Galano, Jean‐Marie; Réversat, Guillaume; Vercauteren, Joseph; Jouhet, Juliette; Maréchal, Éric

doi:10.1104/pp.18.00925

Cited by 37 publications

(38 citation statements)

References 72 publications

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“…In Phaeodactylum tricornutum, a model diatom species, compounds similar to PGs, called isoprostanoids, have been reported, despite the absence of COX sequence annotated in the genome. This finding suggests the existence of an alternative, non-enzymatic, origin of this class of compounds 22 .…”

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confidence: 76%

“…Also, the close proximity of bacterial and diatom sequences and the topology of the tree we present, questions whether diatoms acquired the genes coding for COX via lateral gene transfer 35 , which occurred during diatom evolution [36][37][38] or whether these genes were acquired during endosymbiotic events, at least for species like S. marinoi possessing both α-DOX-like and COX-like enzymes. In the case of T. rotula, α-DOX-like is absent, while the pennate model diatom Phaeodactylum tricornutum completely lacks the enzymatic pathway leading to prostaglandins though it can produce isoprostanoids non-enzymatically 22 . Indeed, the ability to synthesize eicosanoids, including lipoxygenase-derived oxylipins and aldehydes, is not robustly conserved in diatoms 39,40 where genes involved in these metabolisms might have been lost during evolution.…”

Section: Discussionmentioning

confidence: 99%

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Variation in prostaglandin metabolism during growth of the diatom Thalassiosira rotula

Dato

Barbarinaldi

Amato

et al. 2020

Sci Rep

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prostaglandins (pGs) are hormone-like mediators in many physiological and pathological processes that are present in all vertebrates, in some terrestrial and aquatic invertebrates, and have also been identified in some macroalgae. They have recently been reported also in marine microalgae but their role as chemical mediators is largely unknown. Here we studied the expression pattern of the PG biosynthetic pathway during different growth phases of the centric diatom Thalassiosira rotula and assessed the release of PGs in the surrounding environment for the first time. We show that enzymes responsible for PGs formation such as cyclooxygenase, prostaglandin E synthase 2-like and prostaglandin F synthase are mainly expressed at the end of the exponential phase and that PGs are released especially during the stationary and senescent phases, suggesting a possible signaling function for these compounds. Phylogenetic analysis of the limiting enzyme, COX, indicate the presence in diatoms of more than one enzyme related to the oxidative metabolism of fatty acids belonging to the peroxidase-cyclooxygenase superfamily. These findings suggest a more complex evolution and diversity of metabolic pathways leading to the synthesis of lipid mediators in diatoms. Arachidonic acid (ARA), eicosapentaenoic acid (EPA), eicosatrienoic acid (ETrA) and docosahexaenoic acid (DHA) are polyunsaturated fatty acids that are physiologically important for animals at all taxonomic levels, including humans. EPA and DHA contribute to the healthy functioning of the cardiovascular system 1 and are precursors of important classes of fatty acid-derivatives playing multiple signaling roles in inflammation and immune responses, platelet aggregation and tumor growth 2,3. Among these, the inflammation process is one of the most important mechanisms adopted by organisms in response to various external stimuli 3. Inflammation involves a complex interplay of signaling molecules whose final goal is to restore the healthy status of a cell or tissue. Consequences of sustained inflammation are indeed the development of serious diseases such as cancer and autoimmune disorders 4. Included in the eicosanoids are prostaglandins (PGs) synthesized principally from arachidonic acid (ARA) in animals, but also from EPA and ETrA, through the enzymatic route initiated by cyclooxygenase (COXs) enzymes 5. PGs are molecules with a hormone-like behavior playing a prominent role in many physiological processes that have been principally studied in animals 3. The expression of the COXs enzymes is mandatory for their synthesis. COXs exist in two isoforms that differ for their subcellular localization and for their expression timing. COX-1 is located in the endoplasmic reticulum and is constitutively expressed at constant levels in many tissues unless external cues, such as tumor promoting factor, cytokine and growth factor, induce an increase in its expression level. COX-2 is the inducible form, which is not detectable unless a trigger similar to those that stimulate COX-1 express...

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confidence: 76%

Section: Discussionmentioning

confidence: 99%

Variation in prostaglandin metabolism during growth of the diatom Thalassiosira rotula

Dato

Barbarinaldi

Amato

et al. 2020

Sci Rep

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“…Additionally, the nonenzymatic oxylipin biosynthesis is primarily triggered by the oxidative stress and free-radical-catalysed mechanisms. The free radical OH can trigger lipid peroxidation by hydrogen abstraction from polyunsaturated fatty acids and addition of molecular oxygen to form a peroxyl radical (Grun et al, 2007;Gobel and Feussner, 2009;Mueller and Berger, 2009;Lupette et al, 2018). In the previous report, it was demonstrated that the exposure of fungal strain to H 2 O 2 might lead to the altered level of oxidized forms of FAs or oxylipins (Collins et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

Antioxidant‐related catalase CTA1 regulates development, aflatoxin biosynthesis, and virulence in pathogenic fungus Aspergillus flavus

Zhu

Yang

Bai

et al. 2020

Environmental Microbiology

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Summary Reactive oxygen species (ROS) induce the synthesis of a myriad of secondary metabolites, including aflatoxins. It raises significant concern as it is a potent environmental contaminant. In Aspergillus flavus., antioxidant enzymes link ROS stress response with coordinated gene regulation of aflatoxin biosynthesis. In this study, we characterized the function of a core component of the antioxidant enzyme catalase (CTA1) of A. flavus. Firstly, we verified the presence of cta1 corresponding protein (CTA1) by Western blot analysis and mass‐spectrometry based analysis. Then, the functional study revealed that the growth, sporulation and sclerotia formation significantly increased, while aflatoxins production and virulence were decreased in the cta1 deletion mutant as compared with the WT and complementary strains. Furthermore, the absence of the cta1 gene resulted in a significant rise in the intracellular ROS level, which in turn added to the oxidative stress level of cells. A further quantitative proteomics investigation hinted that in vivo, CTA1 might maintain the ROS level to facilitate the aflatoxin synthesis. All in all, the pleiotropic phenotype of A. flavus CTA1 deletion mutant revealed that the antioxidant system plays a crucial role in fungal development, aflatoxins biosynthesis and virulence.

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“…This work suggested that nonenzymatic oxylipins in P. Recently [17], we have investigated variations in the isoprostanoid contents of red and brown macroalgae after exposure to oxidative (heavy metal) stress conditions [18]. In addition, changes in the production of isoprostanoids derived from C18, C20 and C22 fatty acids were observed in the microalga Phaeodatylum tricornutum subjected to oxidative stress by cultivation under increasing doses of hydrogen peroxide (H2O2) [19]. This work suggested that nonenzymatic oxylipins in P. Recently [17], we have investigated variations in the isoprostanoid contents of red and brown macroalgae after exposure to oxidative (heavy metal) stress conditions [18].…”

Section: Introductionmentioning

confidence: 99%

Isoprostanoid Profiling of Marine Microalgae

et al. 2020

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Algae result from a complex evolutionary history that shapes their metabolic network. For example, these organisms can synthesize different polyunsaturated fatty acids, such as those found in land plants and oily fish. Due to the presence of numerous double-bonds, such molecules can be oxidized nonenzymatically, and this results in the biosynthesis of high-value bioactive metabolites named isoprostanoids. So far, there have been only a few studies reporting isoprostanoid productions in algae. To fill this gap, the current investigation aimed at profiling isoprostanoids by liquid chromatography -mass spectrometry/mass spectrometry (LC-MS/MS) in four marine microalgae. A good correlation was observed between the most abundant polyunsaturated fatty acids (PUFAs) produced by the investigated microalgal species and their isoprostanoid profiles. No significant variations in the content of oxidized derivatives were observed for Rhodomonas salina and Chaetoceros gracilis under copper stress, whereas increases in the production of C18-, C20- and C22-derived isoprostanoids were monitored in Tisochrysis lutea and Phaeodactylum tricornutum. In the presence of hydrogen peroxide, no significant changes were observed for C. gracilis and for T. lutea, while variations were monitored for the other two algae. This study paves the way to further studying the physiological roles of isoprostanoids in marine microalgae and exploring these organisms as bioresources for isoprostanoid production.

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Non-Enzymatic Synthesis of Bioactive Isoprostanoids in the Diatom Phaeodactylum following Oxidative Stress

Cited by 37 publications

References 72 publications

Variation in prostaglandin metabolism during growth of the diatom Thalassiosira rotula

Variation in prostaglandin metabolism during growth of the diatom Thalassiosira rotula

Antioxidant‐related catalase CTA1 regulates development, aflatoxin biosynthesis, and virulence in pathogenic fungus Aspergillus flavus

Isoprostanoid Profiling of Marine Microalgae

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