Phosphorus starvation induces membrane remodeling and recycling in <i>Emiliania huxleyi</i>

Shemi, Adva; Schatz, Daniella; Fredricks, Helen F.; Mooy, Benjamin A. S. Van; Porat, Ziv; Vardi, Assaf

doi:10.1111/nph.13940

Cited by 71 publications

(69 citation statements)

References 83 publications

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“…Whether the 2P cells increase gene expression and the synthesis of P-free membrane lipids just to keep steady as cells grow in size or if the cells increase these lipid classes before P restriction is unclear. However, cell size increase as a P-stress response was observed in several other algae but not in P. tricornutum, which also showed increased SQDG synthesis and SQDG increase in cellbased calculations (Abdullahi et al, 2006;Abida et al, 2015;Peter and Sommer, 2015;Shemi et al, 2016). Cañavate et al (2017b) also saw a decline of DGDG content in N. gaditana, whereas our study showed an increase of DGDG in N. oceanica.…”

Section: P-free Lipid Synthesis During Exponential Growthcontrasting

confidence: 62%

“…Whether lipid classes in algae are remodeled during the transition to P limitation or if there is a switch in the synthesis of lipid classes (Brandsma, 2016), and which genes trigger these responses (Shemi et al, 2016), are unresolved questions. Our study addresses these questions and provides a comprehensive scheme for phospholipid-recycling by employing complementary lipidomic and transcriptomic data.…”

Section: Discussionmentioning

confidence: 99%

“…These studies showed a taxonomically diverse lipid response under P stress with unresolved questions related to the diversified mechanism behind the lipid responses. So far, only cursory insights into the lipidremodeling process have been provided by either transcriptomic or lipidomic studies on P limitation (Riekhof et al, 2005;Cruz de Carvalho et al, 2016;Shemi et al, 2016;Cañavate et al, 2017b). To capture the taxonomically diverse response and niche partitioning, studies include ecological successful algae, such as Emiliania huxleyi and Thalassiosira pseudonana (Lessard et al, 2005;Van Mooy et al, 2009), and algae featuring high resilience and lipid content during low P, like Phaeodactylum tricornutum and Nannochloropsis spp.…”

mentioning

confidence: 99%

“…Therefore, it is still unclear by changes of lipid classes if there is a switch in lipid class synthesis or rather a shift of lipid classes (Brandsma, 2016). And what are their regulation patterns (Shemi et al, 2016)? Our study aims to answer parts of these questions through a combined analysis of lipidome and transcriptome data in the highly oleaginous alga Nannochloropsis oceanica.…”

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confidence: 99%

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Mechanisms of Phosphorus Acquisition and Lipid Class Remodeling under P Limitation in a Marine Microalga

et al. 2017

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. Previous studies point to P limitation-induced changes in lipid composition. As, in microalgae, the molecular mechanisms of this specific P stress adaptation remain unresolved, we reveal a detailed phospholipid-recycling scheme in Nannochloropsis oceanica and describe important P acquisition genes based on highly corresponding transcriptome and lipidome data. Initial responses to P limitation showed increased expression of genes involved in P uptake and an expansion of the P substrate spectrum based on purple acid phosphatases. Increase in P trafficking displayed a rearrangement between compartments by supplying P to the chloroplast and carbon to the cytosol for lipid synthesis. We propose a novel phospholipid-recycling scheme for algae that leads to the rapid reduction of phospholipids and synthesis of the P-free lipid classes. P mobilization through membrane lipid degradation is mediated mainly by two glycerophosphoryldiester phosphodiesterases and three patatin-like phospholipases A on the transcriptome level. To compensate for low phospholipids in exponential growth, N. oceanica synthesized sulfoquinovosyldiacylglycerol and diacylglyceroltrimethylhomoserine. In this study, it was shown that an N. oceanica strain has a unique repertoire of genes that facilitate P acquisition and the degradation of phospholipids compared with other stramenopiles. The novel phospholipid-recycling scheme opens new avenues for metabolic engineering of lipid composition in algae.Phosphorus (P) availability is often a limiting factor in aquatic ecosystems (Van Mooy et al., 2009). In some microalgae, nutrient starvation limits cell division and leads to the accumulation of organic carbon (e.g. in the form of triacylglycerols [TAGs]). To cope with P limitation, the interplay of P recycling and changes in lipid classes is observed in the open sea and in culture studies of several stramenopiles and green algae (Van Mooy et al., 2009;Martin et al., 2011;Cañavate et al., 2017b). These studies showed a taxonomically diverse lipid response under P stress with unresolved questions related to the diversified mechanism behind the lipid responses. So far, only cursory insights into the lipidremodeling process have been provided by either transcriptomic or lipidomic studies on P limitation (Riekhof et al., 2005;Cruz de Carvalho et al., 2016;Shemi et al., 2016;Cañavate et al., 2017b). To capture the taxonomically diverse response and niche partitioning, studies include ecological successful algae, such as Emiliania huxleyi and Thalassiosira pseudonana (Lessard et al., 2005;Van Mooy et al., 2009), and algae featuring high resilience and lipid content during low P, like Phaeodactylum tricornutum and Nannochloropsis spp. (Rodolfi et al., 2009;Yang et al., 2013;Mayers et al., 2014;Abida et al., 2015). During these studies, focus is often on changes of long-chain fatty acids (FAs) and their contribution to lipid classes in specific pathways [OPEN] Articles can be viewed without a subscription. www.plantphysiol.org/cgi

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Section: P-free Lipid Synthesis During Exponential Growthcontrasting

confidence: 62%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Mechanisms of Phosphorus Acquisition and Lipid Class Remodeling under P Limitation in a Marine Microalga

et al. 2017

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“…The changed lipid composition under P‐starvation is likely derived from the fact that cells need to dissipate photosynthate and reduction equivalents by means of lipogenesis, as is also observed in other microalgae, e.g., Chlamydomonas reinhardtii (Kamalanathan et al ). Along with other phytoplankton, E. huxleyi has a highly dynamic membrane lipid composition that can be adjusted by environmental stimuli within time‐frames of 1 d, e.g., replacing phospholipids with betaine lipids during P‐starvation (van Mooy et al ; McKew et al ; Shemi et al ).…”

Section: Discussionmentioning

confidence: 99%

Phosphorus and nitrogen starvation reveal life‐cycle specific responses in the metabolome of Emiliania huxleyi (Haptophyta)

Wördenweber

Rokitta

Heidenreich

et al. 2017

Limnology & Oceanography

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The coccolithophore Emiliania huxleyi is a microalga with biogeochemical and biotechnological relevance, due to its high abundance in the ocean and its ability to form intricate calcium carbonate structures. Depletion of macronutrients in oceanic waters is very common and will likely enhance with advancing climate change. We present the first comprehensive metabolome study analyzing the effect of phosphorus (P) and nitrogen (N) starvation on the diploid and haploid life‐cycle stage, applying various metabolome analysis methods to gain new insights in intracellular mechanisms to cope with nutrient starvation. P‐starvation led to an accumulation of many generic and especially N‐rich metabolites, including lipids, osmolytes, and pigments. This suggests that P‐starvation primarily arrests cell‐cycling due to lacking P for nucleic acid synthesis, but that enzymatic functionality is widely preserved. Also, the de‐epoxidation ratio of the xanthophyll cycle was upregulated in the diploid stage under P‐starvation, indicating increased nonphotochemical quenching, a response typically observed under high light stress. In contrast, N‐starvation resulted in a decrease of most central metabolites, also P‐containing ones, especially in the diploid stage, indicating that most enzymatic functionality ceased. The two investigated nutrient starvation conditions caused significantly different responses, contrary to previous assumptions derived from transcriptomic studies. Data highlight that instantaneous biochemical flux is a more dominant driver of the metabolome than the transcriptomically rearranged pathway patterns. Due to the fundamental nature of the observed responses it may be speculated that microalgae with similar nutrient requirements can cope better with P‐starvation than with N‐starvation.

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Metabolism and autophagy in plants—a perfect match

et al. 2022

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Autophagy is a eukaryotic cellular transport mechanism that delivers intracellular macromolecules, proteins, and even organelles to a lytic organelle (vacuole in yeast and plants/lysosome in animals) for degradation and nutrient recycling. The process is mediated by highly conserved autophagy-related (ATG) proteins. In plants, autophagy maintains cellular homeostasis under favorable conditions, guaranteeing normal plant growth and fitness. Severe stress such as nutrient starvation and plant senescence further induce it, thus ensuring plant survival under unfavorable conditions by providing nutrients through the removal of damaged or aged proteins, or organelles. In this article, we examine the interplay between metabolism and autophagy, focusing on the different aspects of this reciprocal relationship. We show that autophagy has a strong influence on a range of metabolic processes, whereas at the same time, even single metabolites can activate autophagy. We highlight the involvement of ATG genes in metabolism, examine the role of the macronutrients carbon and nitrogen, and various micronutrients, and take a closer look at how the interaction between autophagy and metabolism impacts on plant phenotypes and yield.

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Phosphorus starvation induces membrane remodeling and recycling in Emiliania huxleyi

Cited by 71 publications

References 83 publications

Mechanisms of Phosphorus Acquisition and Lipid Class Remodeling under P Limitation in a Marine Microalga

Mechanisms of Phosphorus Acquisition and Lipid Class Remodeling under P Limitation in a Marine Microalga

Phosphorus and nitrogen starvation reveal life‐cycle specific responses in the metabolome of Emiliania huxleyi (Haptophyta)

Metabolism and autophagy in plants—a perfect match

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