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      Molecular adaptations to phosphorus deprivation and comparison with nitrogen deprivation responses in the diatom Phaeodactylum tricornutum

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          Abstract

          Phosphorus, an essential element for all living organisms, is a limiting nutrient in many regions of the ocean due to its fast recycling. Changes in phosphate (P i) availability in aquatic systems affect diatom growth and productivity. We investigated the early adaptive mechanisms in the marine diatom Phaeodactylum tricornutum to P deprivation using a combination of transcriptomics, metabolomics, physiological and biochemical experiments. Our analysis revealed strong induction of gene expression for proteins involved in phosphate acquisition and scavenging, and down-regulation of processes such as photosynthesis, nitrogen assimilation and nucleic acid and ribosome biosynthesis. P deprivation resulted in alterations of carbon allocation through the induction of the pentose phosphate pathway and cytosolic gluconeogenesis, along with repression of the Calvin cycle. Reorganization of cellular lipids was indicated by coordinated induced expression of phospholipases, sulfolipid biosynthesis enzymes and a putative betaine lipid biosynthesis enzyme. A comparative analysis of nitrogen- and phosphorus-deprived P. tricornutum revealed both common and distinct regulation patterns in response to phosphate and nitrate stress. Regulation of central carbon metabolism and amino acid metabolism was similar, whereas unique responses were found in nitrogen assimilation and phosphorus scavenging in nitrogen-deprived and phosphorus-deprived cells, respectively.

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Biogeochemical Controls and Feedbacks on Ocean Primary Production

            Changes in oceanic primary production, linked to changes in the network of global biogeochemical cycles, have profoundly influenced the geochemistry of Earth for over 3 billion years. In the contemporary ocean, photosynthetic carbon fixation by marine phytoplankton leads to formation of approximately 45 gigatons of organic carbon per annum, of which 16 gigatons are exported to the ocean interior. Changes in the magnitude of total and export production can strongly influence atmospheric CO2 levels (and hence climate) on geological time scales, as well as set upper bounds for sustainable fisheries harvest. The two fluxes are critically dependent on geophysical processes that determine mixed-layer depth, nutrient fluxes to and within the ocean, and food-web structure. Because the average turnover time of phytoplankton carbon in the ocean is on the order of a week or less, total and export production are extremely sensitive to external forcing and consequently are seldom in steady state. Elucidating the biogeochemical controls and feedbacks on primary production is essential to understanding how oceanic biota responded to and affected natural climatic variability in the geological past, and will respond to anthropogenically influenced changes in coming decades. One of the most crucial feedbacks results from changes in radiative forcing on the hydrological cycle, which influences the aeolian iron flux and, in turn, affects nitrogen fixation and primary production in the oceans.
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              A Model for Carbohydrate Metabolism in the Diatom Phaeodactylum tricornutum Deduced from Comparative Whole Genome Analysis

              Background Diatoms are unicellular algae responsible for approximately 20% of global carbon fixation. Their evolution by secondary endocytobiosis resulted in a complex cellular structure and metabolism compared to algae with primary plastids. Methodology/Principal Findings The whole genome sequence of the diatom Phaeodactylum tricornutum has recently been completed. We identified and annotated genes for enzymes involved in carbohydrate pathways based on extensive EST support and comparison to the whole genome sequence of a second diatom, Thalassiosira pseudonana. Protein localization to mitochondria was predicted based on identified similarities to mitochondrial localization motifs in other eukaryotes, whereas protein localization to plastids was based on the presence of signal peptide motifs in combination with plastid localization motifs previously shown to be required in diatoms. We identified genes potentially involved in a C4-like photosynthesis in P. tricornutum and, on the basis of sequence-based putative localization of relevant proteins, discuss possible differences in carbon concentrating mechanisms and CO2 fixation between the two diatoms. We also identified genes encoding enzymes involved in photorespiration with one interesting exception: glycerate kinase was not found in either P. tricornutum or T. pseudonana. Various Calvin cycle enzymes were found in up to five different isoforms, distributed between plastids, mitochondria and the cytosol. Diatoms store energy either as lipids or as chrysolaminaran (a β-1,3-glucan) outside of the plastids. We identified various β-glucanases and large membrane-bound glucan synthases. Interestingly most of the glucanases appear to contain C-terminal anchor domains that may attach the enzymes to membranes. Conclusions/Significance Here we present a detailed synthesis of carbohydrate metabolism in diatoms based on the genome sequences of Thalassiosira pseudonana and Phaeodactylum tricornutum. This model provides novel insights into acquisition of dissolved inorganic carbon and primary metabolic pathways of carbon in two different diatoms, which is of significance for an improved understanding of global carbon cycles.
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                Author and article information

                Contributors
                Role: InvestigationRole: Writing – original draft
                Role: Data curationRole: Formal analysisRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: Investigation
                Role: ConceptualizationRole: Data curationRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: Project administrationRole: SupervisionRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                23 February 2018
                2018
                : 13
                : 2
                : e0193335
                Affiliations
                [001]Cell, Molecular Biology and Genomics Group, Department of Biology, Norwegian University of Science and Technology, Trondheim, Norway
                University of Connecticut, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-0544-7437
                Article
                PONE-D-17-12290
                10.1371/journal.pone.0193335
                5825098
                29474408
                2efb6ed0-6186-4772-8505-082a33893041
                © 2018 Alipanah et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 29 March 2017
                : 8 February 2018
                Page count
                Figures: 7, Tables: 1, Pages: 24
                Funding
                Funded by: Norwegian Research Council
                Award ID: 238851 and 234229
                Award Recipient :
                This work was supported by grants from 238851 and 234229 from the Research Council of Norway to AMB and a PhD grant from the Norwegian University of Science and Technology to LA.
                Categories
                Research Article
                Biology and Life Sciences
                Genetics
                Gene Expression
                Gene Regulation
                Biology and Life Sciences
                Organisms
                Eukaryota
                Plants
                Algae
                Phytoplankton
                Diatoms
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Plankton
                Phytoplankton
                Diatoms
                Physical Sciences
                Chemistry
                Chemical Compounds
                Phosphates
                Biology and Life Sciences
                Biochemistry
                Biosynthesis
                Biology and Life Sciences
                Biochemistry
                Metabolism
                Metabolites
                Biology and Life Sciences
                Biochemistry
                Lipids
                Biology and Life Sciences
                Biochemistry
                Plant Biochemistry
                Photosynthesis
                Biology and Life Sciences
                Plant Science
                Plant Biochemistry
                Photosynthesis
                Physical Sciences
                Materials Science
                Materials by Attribute
                Pigments
                Custom metadata
                The study is MIAME compliant. Raw data have been deposited in GEO (accession GSE66063).

                Uncategorized
                Uncategorized

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