Current trends to comprehend lipid metabolism in diatoms

Progress in Lipid Research - Tập 70 - Trang 1-16 - 2018
Nodumo Nokulunga Zulu1, Krzysztof Zienkiewicz1, Katharina Vollheyde1, Ivo Feussner1,2
1University of Goettingen, Albrecht-von-Haller-Institute for Plant Sciences, Department of Plant Biochemistry, 37077 Goettingen, Germany
2University of Goettingen, Goettingen Center for Molecular Biosciences (GZMB), Department of Plant Biochemistry, 37077 Goettingen, Germany

Tài liệu tham khảo

Obata, 2013, The central carbon and energy metabolism of marine diatoms, Meta, 3, 325 Tesson, 2013, Characterization and localization of insoluble organic matrices associated with diatom cell walls: insight into their roles during cell wall formation, PLoS One, 8, e61675, 10.1371/journal.pone.0061675 Wilhelm, 2006, The regulation of carbon and nutrient assimilation in diatoms is dignificantly different from green algae, Protist, 157, 91, 10.1016/j.protis.2006.02.003 Zaslavskaia, 2000, Transformation of the diatom Phaeodactylum tricornutum (Bacillariophyceae) with a variety of selectable marker and reporter genes, J Phycol, 36, 379, 10.1046/j.1529-8817.2000.99164.x Gruber, 2015, Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage, Plant J, 81, 519, 10.1111/tpj.12734 Scala, 2002, Genome properties of the diatom Phaeodactylum tricornutum, Plant Physiol, 129, 993, 10.1104/pp.010713 Levitan, 2014, Diatoms: a fossil fuel of the future, Trends Biotechnol, 32, 117, 10.1016/j.tibtech.2014.01.004 De Martino, 2007, Genetic and phenotypic characterization of Phaeodactylum tricornutum (Bacillariophyceae) accessions, J Phycol, 43, 992, 10.1111/j.1529-8817.2007.00384.x Armbrust, 2004, The genome of the diatom Thalassiosira pseudonana: Ecology, evolution, and metabolism, Science, 306, 79, 10.1126/science.1101156 Rastogi, 2015, Probing the evolutionary history of epigenetic mechanisms: what can we learn from marine diatoms, AIMS Genet, 2, 173, 10.3934/genet.2015.3.173 Domergue, 2003, New insight into Phaeodactylum tricornutum fatty acid metabolism. Cloning and functional characterization of plastidial and microsomal Δ12-fatty acid desaturases, Plant Physiol, 131, 1648, 10.1104/pp.102.018317 Theriot, 2010, A preliminary multigene phylogeny of the diatoms (Bacillariophyta): challenges for future research, Plant Ecol Evol, 143, 278, 10.5091/plecevo.2010.418 Vardi, 2009, Diatom genomes come of age, Genome Biol v, 9, 1829 Merz, 2014, 1 Apt, 2002, In vivo characterization of diatom multipartite plastid targeting signals, J Cell Sci, 115, 4061, 10.1242/jcs.00092 Kroth, 2008, A model for carbohydrate metabolism in the diatom Phaeodactylum tricornutum deduced from comparative whole genome analysis, PLoS One, 3, 10.1371/journal.pone.0001426 Granum, 2002, Cellular and extracellular production of carbohydrates and amino acids by the marine diatom Skeletonema costatum diel variations and effects of N depletion, Mar Ecol Prog Ser, 242, 83, 10.3354/meps242083 Guschina, 2006, Lipids and lipid metabolism in eukaryotic algae, Prog Lipid Res, 45, 160, 10.1016/j.plipres.2006.01.001 Fu, 2015, Developing diatoms for value-added products: challenges and opportunities, New Biotechnol, 32, 547, 10.1016/j.nbt.2015.03.016 Vílchez, 2011, Marine carotenoids: Biological functions and commercial applications, Mar Drugs, 9, 319, 10.3390/md9030319 Spolaore, 2006, Commercial applications of microalgae, J Biosci Bioeng, 101, 87, 10.1263/jbb.101.87 Ramachandra, 2009, Milking diatoms for sustainable energy: Biochemical engineering versus gasoline-secreting diatom solar panels, Ind Eng Chem Res, 48, 8769, 10.1021/ie900044j Hemaiswarya, 2011, Microalgae: a sustainable feed source for aquaculture, World J Microbiol Biotechnol, 27, 1737, 10.1007/s11274-010-0632-z Lebeau, 2003, Diatom cultivation and biotechnologically relevant products. Part I: Cultivation at various scales, Appl Microbiol Biotechnol, 60, 612, 10.1007/s00253-002-1176-4 Tonon, 2002, Long chain polyunsaturated fatty acid production and partitioning to triacylglycerols in four microalgae, Phytochemistry, 61, 15, 10.1016/S0031-9422(02)00201-7 Yi, 2017, Exploring valuable lipids in diatoms, Front Mar Sci, 4, 1, 10.3389/fmars.2017.00017 Maheswari, 2005, The diatom EST database, Nucleic Acids Res, 33, D344, 10.1093/nar/gki121 Bowler, 2008, The Phaeodactylum genome reveals the evolutionary history of diatom genomes, Nature, 456, 239, 10.1038/nature07410 Liang, 2014, Profiling of fatty acid methyl esters from the oleaginous diatom Fistulifera sp. strain JPCC DA0580 under nutrition-sufficient and -deficient conditions, J Appl Phycol, 26, 2295, 10.1007/s10811-014-0265-y Li, 2014, Biochemical and genetic engineering of diatoms for polyunsaturated fatty acid biosynthesis, Mar Drugs, 12, 153, 10.3390/md12010153 Dunahay, 1995, Genetic transformation of the diatoms Cyclotella cryptica and Navicula saprophila, J Phycol, 31, 1004, 10.1111/j.0022-3646.1995.01004.x Lang, 2011, Fatty acid profiles and their distribution patterns in microalgae: a comprehensive analysis of more than 2000 strains from the SAG culture collection, BMC Plant Biol, 11, 124, 10.1186/1471-2229-11-124 Sapriel, 2009, Genome-wide transcriptome analyses of silicon metabolism in Phaeodactylum tricornutum reveal the multilevel regulation of silicic acid transporters, PLoS One, 4, 10.1371/journal.pone.0007458 Kira, 2016, Nuclear transformation of the diatom Phaeodactylum tricornutum using PCR-amplified DNA fragments by microparticle bombardment, Mar Genomics, 25, 49, 10.1016/j.margen.2015.12.004 Daboussi, 2014, Genome engineering empowers the diatom Phaeodactylum tricornutum for biotechnology, Nat Commun, 5, 3831, 10.1038/ncomms4831 Ohlrogge, 1995, Lipid biosynthesis, Plant Cell, 7, 957, 10.1105/tpc.7.7.957 Hu, 2008, Microalgal triacylglycerols as feedstocks for biofuel production: perspectives and advances, Plant J, 54, 621, 10.1111/j.1365-313X.2008.03492.x Tanaka, 2015, Oil accumulation by the oleaginous diatom Fistulifera solaris as revealed by the genome and transcriptome, Plant Cell, 27, 162, 10.1105/tpc.114.135194 Ke, 2000, The role of pyruvate dehydrogenase and acetyl-coenzyme A synthetase in fatty acid synthesis in developing arabidopsis seeds, Plant Physiol, 123, 497, 10.1104/pp.123.2.497 Leonardi, 2005, Coenzyme A: Back in action, Prog Lipid Res, 44, 125, 10.1016/j.plipres.2005.04.001 Lin, 2008, The role of acetyl-coenzyme A synthetase in Arabidopsis, Plant Physiol, 147, 1822, 10.1104/pp.108.121269 Ma, 2014, Antisense knockdown of pyruvate dehydrogenase kinase promotes the neutral lipid accumulation in the diatom Phaeodactylum tricornutum, Microb Cell Factories, 13, 100 Flori, 2016, Ultrastructure of the periplastidial compartment of the diatom Phaeodactylum tricornutum, Protist, 167, 254, 10.1016/j.protis.2016.04.001 Huerlimann, 2013, Comprehensive guide to acetyl-carboxylases in algae, Crit Rev Biotechnol, 33, 49, 10.3109/07388551.2012.668671 Roessler, 1990, Purification and characterization of acetyl-CoA carboxylase from the diatom Cyclotella cryptica, Plant Physiol, 92, 73, 10.1104/pp.92.1.73 Roessler, 1993, Cloning and characterization of the gene that encodes acetyl-coenzyme A carboxylase in the alga Cyclotella cryptica, J Biol Chem, 268, 19254, 10.1016/S0021-9258(19)36507-X Xie, 2013, Functional characterization of an ACCase subunit from the diatom Phaeodactylum tricornutum expressed in Escherichia coli, Biotechnol Appl Biochem, 60, 330, 10.1002/bab.1091 Ryall, 2003, Plastid-derived type II fatty acid biosynthetic enzymes in chromists, Gene, 313, 139, 10.1016/S0378-1119(03)00671-1 Li-Beisson, 2010, 1 Dolch, 2017, A palmitic acid elongase affects eicosapentaenoic acid and plastidial monogalactosyldiacylglycerol levels in Nannochloropsis, Plant Physiol, 173, 742, 10.1104/pp.16.01420 Koo, 2004, On the export of fatty acids from the chloroplast, J Biol Chem, 279, 16101, 10.1074/jbc.M311305200 Chapman, 2012, Compartmentation of triacylglycerol accumulation in plants, J Biol Chem, 287, 2288, 10.1074/jbc.R111.290072 Gong, 2011, Characterization of a novel thioesterase (PtTE) from Phaeodactylum tricornutum, J Basic Microbiol, 51, 666, 10.1002/jobm.201000520 Botella, 2017, Importance of phosphatidylcholine on the chloroplast surface, Prog Lipid Res, 65, 12, 10.1016/j.plipres.2016.11.001 Tjellström, 2012, Rapid Kinetic Labeling of Arabidopsis Cell Suspension Cultures: Implications for Models of Lipid Export from Plastids, Plant Physiol, 158, 601, 10.1104/pp.111.186122 Kroth, 2002, Protein transport into secondary plastids and the evolution of primary and secondary plastids, Int Rev Cytol, 221, 191, 10.1016/S0074-7696(02)21013-X Moriyama, 2018, Revisiting the algal “chloroplast lipid droplet”: the absence of an entity that is unlikely to exist, Plant Physiol, 176, 1519, 10.1104/pp.17.01512 Du, 2016, Triacylglycerol accumulation in photosynthetic cells in plants and algae, 179 Xu, 2016, Cellular organization of triacylglycerol biosynthesis in microalgae, 207 Cagliari, 2011, Biosynthesis of triacylglycerols (TAGs) in plants and algae, Internatl J Plant Biol, 2, 10, 10.4081/pb.2011.e10 Li-Beisson, 2016, Lipids: From chemical structures, biosynthesis, and analyses to industrial applications, 1 Yu, 2011, Modifications of the metabolic pathways of lipid and triglyceride production in microalgae, Microb Cell Factories, 10, 91, 10.1186/1475-2859-10-91 Blatti, 2012, Manipulating fatty acid biosynthesis in microalgae for biofuel through protein-protein interactions, PLoS One, 7, e42949, 10.1371/journal.pone.0042949 Liu, 2013, Lipid metabolism in microalgae distinguishes itself, Curr Opin Biotechnol, 24, 300, 10.1016/j.copbio.2012.08.008 Fan, 2013, Phospholipid:diacylglycerol acyltransferase-mediated triacylglycerol biosynthesis is crucial for protection against fatty acid-induced cell death in growing tissues of Arabidopsis, Plant J, 76, 930, 10.1111/tpj.12343 Fan, 2013, Dual role for phospholipid:diacylglycerol acyltransferase: Enhancing fatty acid synthesis and diverting fatty acids from membrane lpids to triacylglycerol in Arabidopsis leaves, Plant Cell, 25, 3506, 10.1105/tpc.113.117358 Oelkers, 2000, A lecithin cholesterol acyltransferase-like gene mediates diacylglycerol esterification in yeast, J Biol Chem, 275, 15609, 10.1074/jbc.C000144200 Oelkers, 2002, The DGA1 gene determines a second triglyceride synthetic pathway in yeast, J Biol Chem, 277, 8877, 10.1074/jbc.M111646200 Gong, 2013, Identification and characterization of PtDGAT2B, an acyltransferase of the DGAT2 acyl-Coenzyme A: Diacylglycerol acyltransferase family in the diatom Phaeodactylum tricornutum, FEBS Lett, 587, 481, 10.1016/j.febslet.2013.01.015 Cui, 2013, Cloning and characterization of a novel diacylglycerol acyltransferase from the diatom Phaeodactylum tricornutum, J Appl Phycol, 25, 1509, 10.1007/s10811-013-9991-9 Bagnato, 2017, Analysis of triglyceride synthesis unveils a green algal soluble diacylglycerol acyltransferase and provides clues to potential enzymatic components of the chloroplast pathway, BMC Genomics, 18, 223, 10.1186/s12864-017-3602-0 Guihéneuf, 2011, Cloning and molecular characterization of a novel acyl-CoA:diacylglycerol acyltransferase 1-like gene (PtDGAT1) from the diatom Phaeodactylum tricornutum, FEBS J, 278, 3651, 10.1111/j.1742-4658.2011.08284.x Khozin-Goldberg, 2016, Microalgae as a source for VLC-PUFA production, 471 Hamilton, 2014, Metabolic engineering of Phaeodactylum tricornutum for the enhanced accumulation of omega-3 long chain polyunsaturated fatty acids, Metab Eng, 22, 3, 10.1016/j.ymben.2013.12.003 Tonon, 2005, Identification of a long-chain polyunsaturated fatty acid acyl-coenzyme A synthetase from the diatom Thalassiosira pseudonana, Plant Physiol, 138, 402, 10.1104/pp.104.054528 Popko, 2016, Metabolome analysis reveals betaine lipids as major source for triglyceride formation, and the accumulation of sedoheptulose during nitrogen-starvation of Phaeodactylum tricornutum, PLoS One, 11, 10.1371/journal.pone.0164673 Mus, 2013, Physiological and molecular analysis of carbon source supplementation and pH stress-induced lipid accumulation in the marine diatom Phaeodactylum tricornutum, Appl Microbiol Biotechnol, 97, 3625, 10.1007/s00253-013-4747-7 Mühlroth, 2013, Pathways of lipid metabolism in marine algae, co-expression network, bottlenecks and candidate genes for enhanced production of EPA and DHA in species of chromista, Mar Drugs, 11, 4662, 10.3390/md11114662 Chapman, 2012, Biogenesis and functions of lipid droplets in plants, J Lipid Res, 53, 215, 10.1194/jlr.R021436 Goold, 2015, Microalgal lipid droplets: composition, diversity, biogenesis and functions, Plant Cell Rep, 34, 545, 10.1007/s00299-014-1711-7 Yoneda, 2016, Identification of a major lipid droplet protein in a marine diatom Phaeodactylum tricornutum, Plant Cell Physiol, 57, 397, 10.1093/pcp/pcv204 Hamilton, 2015, Towards the industrial production of omega-3 long chain polyunsaturated fatty acids from a genetically modified diatom Phaeodactylum tricornutum, PLoS One, 10, 10.1371/journal.pone.0144054 Yang, 2017, Fatty Acid and Lipid Class Composition of the Microalga Phaeodactylum tricornutum, J Oleo Sci, 66, 363, 10.5650/jos.ess16205 Yang, 2013, Molecular and cellular mechanisms of neutral lipid accumulation in diatom following nitrogen deprivation, Biotechnol Biofuels, 6, 67, 10.1186/1754-6834-6-67 Jiang, 2004, Effects of lowering temperature during culture on the production of polyunsaturated fatty acids in the marine diatom Phaeodactylum tricornutum (Bacillariophyeae), J Phycol, 40, 651, 10.1111/j.1529-8817.2004.03112.x Stonik, 2015, Low-molecular-weight metabolites from diatoms: structures, biological roles and biosynthesis, Mar Drugs, 13, 3672, 10.3390/md13063672 Dolch, 2015, Inventory of fatty acid desaturases in the pennate diatom Phaeodactylum tricornutum, Mar Drugs, 13, 1317, 10.3390/md13031317 Domergue, 2003, Acyl carriers used as substrates by the desaturases and elongases involved in very long-chain polyunsaturated fatty acids biosynthesis reconstituted in yeast, J Biol Chem, 278, 35115, 10.1074/jbc.M305990200 Khozin, 1997, Elucidation of the biosynthesis of eicosapentaenoic acid in the microalga Porphyridium cruentum (II. Studies with radiolabeled precursors), Plant Physiol, 114, 223, 10.1104/pp.114.1.223 Sukenik, 1999, 41 Bigogno, 2002, Biosynthesis of arachidonic acid in the oleaginous microalga Parietochloris incisa (Chlorophyceae): radiolabeling studies, Lipids, 37, 209, 10.1007/s11745-002-0882-6 Khozin-Goldberg, 2002, Nitrogen starvation induces the accumulation of arachidonic acid in the freshwater green alga Parietochloris incisa (Trebuxiophyceae), J Phycol, 38, 991, 10.1046/j.1529-8817.2002.01160.x Petroutsos, 2014, Evolution of galactoglycerolipid biosynthetic pathways - From cyanobacteria to primary plastids and from primary to secondary plastids, Prog Lipid Res, 54, 68, 10.1016/j.plipres.2014.02.001 Liang, 2014, Profiling of polar lipids in marine oleaginous diatom Fistulifera solaris JPCC DA0580: prediction of the potential mechanism for eicosapentaenoic acid-incorporation into triacylglycerol, Mar Drugs, 12, 3218, 10.3390/md12063218 Abida, 2015, Membrane glycerolipid remodeling triggered by nitrogen and phosphorus starvation in Phaeodactylum tricornutum, Plant Physiol, 167, 118, 10.1104/pp.114.252395 Yongmanitchai, 1993, Positional distribution of fatty acids, and molecular species of polar lipids, in the diatom Phaeodactylum tricornutum, J Gen Microbiol, 139, 465, 10.1099/00221287-139-3-465 Joyard, 2010, Chloroplast proteomics highlights the subcellular compartmentation of lipid metabolism, Prog Lipid Res, 49, 128, 10.1016/j.plipres.2009.10.003 Apt, 1999, Commercial developments in microalgal biotechnology, J Phycol, 35, 215, 10.1046/j.1529-8817.1999.3520215.x Yodsuwan, 2017, Effect of nitrogen concentration on growth, lipid production and fatty acid profiles of the marine diatom Phaeodactylum tricornutum, Agric Nat Res, 51, 190 Liu, 2009, Effects of organic carbon sources on growth, photosynthesis, and respiration of Phaeodactylum tricornutum, J Appl Phycol, 21, 239, 10.1007/s10811-008-9355-z Wu, 2015, Enzyme activity highlights the importance of the oxidative pentose phosphate pathway in lipid accumulation and growth of Phaeodactylum tricornutum under CO2 concentration, Biotechnol Biofuels, 8, 78, 10.1186/s13068-015-0262-7 Yongmanitchai, 1991, Growth of and omega-3 fatty acid production by Phaeodactylum tricornutum under different culture conditions, Appl Environ Microbiol, 57, 419, 10.1128/AEM.57.2.419-425.1991 Cerón Garcí, 2000, Mixotrophic growth of Phaeodactylum tricornutum on glycerol: growth rate and fatty acid profile, J Appl Phycol, 12, 239, 10.1023/A:1008123000002 Villanova, 2017, Investigating mixotrophic metabolism in the model diatom Phaeodactylum tricornutum, Philos Trans R Soc B, 372, 20160404, 10.1098/rstb.2016.0404 Wang, 2012, A study on lipid production of the mixotrophic microalgae Phaeodactylum tricornutum on various carbon sources, Afr J Microbiol Res, 6, 1041 Fields, 2014, Sources and resources: importance of nutrients, resource allocation, and ecology in microalgal cultivation for lipid accumulation, Appl Microbiol Biotechnol, 98, 4805, 10.1007/s00253-014-5694-7 Khozin-Goldberg, 2006, The effect of phosphate starvation on the lipid and fatty acid composition of the fresh water eustigmatophyte Monodus subterraneus, Phytochemistry, 67, 696, 10.1016/j.phytochem.2006.01.010 Hildebrand, 2017, Effects of chrysolaminarin synthase knockdown in the diatom Thalassiosira pseudonana: implications of reduced carbohydrate storage relative to green algae, Algal Res, 23, 66, 10.1016/j.algal.2017.01.010 Li, 2010, Inhibition of starch synthesis results in overproduction of lipids in Chlamydomonas reinhardtii, Biotechnol Bioeng, 107, 258, 10.1002/bit.22807 Alipanah, 2015, Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum, J Exp Bot, 66, 6281, 10.1093/jxb/erv340 Breuer, 2012, The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains, Bioresour Technol, 124, 217, 10.1016/j.biortech.2012.08.003 Ak, 2015, The effect of stress due to nitrogen limitation on lipid content of Phaeodactylum tricornutum (bohlin) cultured outdoor in photobioreactor, Turk J Fish Aquat Sci, 15, 647, 10.4194/1303-2712-v15_3_09 Remmers, 2017, Dynamics of triacylglycerol and EPA production in Phaeodactylum tricornutum under nitrogen starvation at different light intensities, PLoS One, 12, 10.1371/journal.pone.0175630 Iwai, 2014, Enhancement of extraplastidic oil synthesis in Chlamydomonas reinhardtii using a type-2 diacylglycerol acyltransferase with a phosphorus starvation–inducible promoter, Plant Biotechnol J, 12, 808, 10.1111/pbi.12210 Burrows, 2012, Dynamics of lipid biosynthesis and redistribution in the marine diatom Phaeodactylum tricornutum under nitrate deprivation, BioEnergy Res, 5, 876, 10.1007/s12155-012-9201-7 Yang, 2014, Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum, J Appl Phycol, 26, 73, 10.1007/s10811-013-0050-3 Shen, 2016, Identification of characteristic fatty acids to quantify triacylglycerols in microalgae, Front Plant Sci, 7, 162, 10.3389/fpls.2016.00162 Feng, 2015, Examination of metabolic responses to phosphorus limitation via proteomic analyses in the marine diatom Phaeodactylum tricornutum, Sci Rep, 5 Yang, 2014, Systems-level analysis of the metabolic responses of the diatom Phaeodactylum tricornutum to phosphorus stress, Environ Microbiol, 16, 1793, 10.1111/1462-2920.12411 Chauton, 2013, Gene regulation of carbon fixation, storage, and utilization in the diatom Phaeodactylum tricornutum acclimated to light/dark cycles, Plant Physiol, 161, 1034, 10.1104/pp.112.206177 Yu, 2016, Role of sufficient phosphorus in biodiesel production from diatom Phaeodactylum tricornutum, Appl Microbiol Biotechnol, 100, 6927, 10.1007/s00253-016-7641-2 Adams, 2014, Enhancing lipid production of the marine diatom Chaetoceros gracilis: synergistic interactions of sodium chloride and silicon, J Appl Phycol, 26, 1351, 10.1007/s10811-013-0156-7 Jiang, 2015, Coupled effect of silicate and nickel on the growth and lipid production in the diatom Nitzschia perspicua, J Appl Phycol, 27, 1137, 10.1007/s10811-014-0412-5 Zendejas, 2012, Characterization of the acylglycerols and resulting biodiesel derived from vegetable oil and microalgae (Thalassiosira pseudonana and Phaeodactylum tricornutum), Biotechnol Bioeng, 109, 1146, 10.1002/bit.24395 Hemme, 2014, Systems-wide analysis of acclimation responses to long-term heat stress and recovery in the photosynthetic model organism Chlamydomonas reinhardtii, Plant Cell, 26, 4270, 10.1105/tpc.114.130997 Hemschemeier, 2013, Copper response regulator1–dependent and–independent responses of the Chlamydomonas reinhardtii transcriptome to dark anoxia, Plant Cell, 25, 3186, 10.1105/tpc.113.115741 Kurpan Nogueira, 2015, Impact of temperature and light intensity on triacylglycerol accumulation in marine microalgae, Biomass Bioenergy, 72, 280, 10.1016/j.biombioe.2014.10.017 Dong, 2016, High light stress triggers distinct proteomic responses in the marine diatom Thalassiosira pseudonana, BMC Genomics, 17, 994, 10.1186/s12864-016-3335-5 Bai, 2016, Proteomic analyses bring new insights into the effect of a dark stress on lipid biosynthesis in Phaeodactylum tricornutum, Sci Rep, 6 Dodson, 2014, The long and short of it: temperature-dependent modifications of fatty acid chain length and unsaturation in the galactolipid profiles of the diatoms Haslea ostrearia and Phaeodactylum tricornutum, Hydrobiologia, 727, 95, 10.1007/s10750-013-1790-4 Feijão, 2017, Heat wave impacts on the model diatom Phaeodactylum tricornutum: Searching for photochemical and fatty acid biomarkers of thermal stress, Ecol Indic, 10.1016/j.ecolind.2017.07.058 Radakovits, 2011, Genetic engineering of fatty acid chain length in Phaeodactylum tricornutum, Metab Eng, 13, 89, 10.1016/j.ymben.2010.10.003 Blatti, 2013, Engineering fatty acid biosynthesis in microalgae for sustainable biodiesel, Curr Opin Chem Biol, 17, 496, 10.1016/j.cbpa.2013.04.007 Peng, 2014, Delta 5 fatty acid desaturase upregulates the synthesis of polyunsaturated fatty acids in the marine diatom Phaeodactylum tricornutum, J Agric Food Chem, 62, 8773, 10.1021/jf5031086 Xue, 2015, Genetic improvement of the microalga Phaeodactylum tricornutum for boosting neutral lipid accumulation, Metab Eng, 27, 1, 10.1016/j.ymben.2014.10.002 Yao, 2014, Glycerol and neutral lipid production in the oleaginous marine diatom Phaeodactylum tricornutum promoted by overexpression of glycerol-3-phosphate dehydrogenase, Biotechnol Biofuels, 7, 110, 10.1186/1754-6834-7-110 Herrera-Valencia, 2012, In silico cloning and characterization of the glycerol-3-phosphate dehydrogenase (GPDH) gene family in the green microalga Chlamydomonas reinhardtii, Curr Microbiol, 64, 477, 10.1007/s00284-012-0095-6 Balamurugan, 2017, Occurrence of plastidial triacylglycerol synthesis and the potential regulatory role of AGPAT in the model diatom Phaeodactylum tricornutum, Biotechnol Biofuels, 10, 97, 10.1186/s13068-017-0786-0 Zienkiewicz, 2016, Stress-induced neutral lipid biosynthesis in microalgae — Molecular, cellular and physiological insights, Biochim Biophys Acta, 1861 (, 1269, 10.1016/j.bbalip.2016.02.008 Niu, 2013, Improvement of neutral lipid and polyunsaturated fatty acid biosynthesis by overexpressing a type 2 diacylglycerol acyltransferase in marine diatom Phaeodactylum tricornutum, Mar Drugs, 11, 4558, 10.3390/md11114558 Dinamarca, 2017, Overexpression of a diacylglycerol acyltransferase gene in Phaeodactylum tricornutum directs carbon towards lipid biosynthesis, J Phycol, 53, 405, 10.1111/jpy.12513 Vaezi, 2013, Identification and functional characterization of genes encoding omega-3 polyunsaturated fatty acid biosynthetic activities from unicellular microalgae, Mar Drugs, 11, 5116, 10.3390/md11125116 Wagner, 2010, Identification and characterization of an acyl-CoA:diacylglycerol acyltransferase 2 (DGAT2) gene from the microalga O. tauri, Plant Physiol Biochem, 48, 407, 10.1016/j.plaphy.2010.03.008 Zulu, 2017, Heterologous co-expression of a yeast diacylglycerol acyltransferase (ScDGA1) and a plant oleosin (AtOLEO3) as an efficient tool for enhancing triacylglycerol accumulation in the marine diatom Phaeodactylum tricornutum, Biotechnol Biofuels, 10, 187, 10.1186/s13068-017-0874-1 Vanhercke, 2014, Metabolic engineering of biomass for high energy density: oilseed-like triacylglycerol yields from plant leaves, Plant Biotechnol J, 12, 231, 10.1111/pbi.12131 Kelly, 2013, Suppression of the SUGAR-DEPENDENT1 triacylglycerol lipase family during seed development enhances oil yield in oilseed rape (Brassica napus L.), Plant Biotechnol J, 11, 355, 10.1111/pbi.12021 Eastmond, 2006, SUGAR-DEPENDENT1 encodes a patatin domain triacylglycerol lipase that initiates storage oil breakdown in germinating Arabidopsis seeds, Plant Cell, 18, 665, 10.1105/tpc.105.040543 Trentacoste, 2013, Metabolic engineering of lipid catabolism increases microalgal lipid accumulation without compromising growth, Proc Natl Acad Sci U S A, 110, 19748, 10.1073/pnas.1309299110 Barka, 2016, Identification of a triacylglycerol lipase in the diatom Phaeodactylum tricornutum, Biochim Biophys Acta, 1861, 239, 10.1016/j.bbalip.2015.12.023 Siaut, 2007, Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum, Gene, 406, 23, 10.1016/j.gene.2007.05.022 Allen, 2008, Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation, Proc Natl Acad Sci U S A, 105, 10438, 10.1073/pnas.0711370105 Bertrand, 2015, Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge, Proc Natl Acad Sci U S A, 112, 9938, 10.1073/pnas.1501615112 Hockin, 2012, The response of diatom central carbon metabolism to nitrogen starvation is different from that of green algae and higher plants, Plant Physiol, 158, 299, 10.1104/pp.111.184333 Galachyants, 2011, Complete chloroplast genome sequence of freshwater araphid pennate diatom alga Synedra acus from Lake Baikal, Int J Biol, 4, 27, 10.5539/ijb.v4n1p27 Kowallik, 1995, The chloroplast genome of a chlorophyll a+ c-containing alga, Odontella sinensis, Plant Mol Biol Report, 13, 336, 10.1007/BF02669188 Oudot-Le Secq, 2007, Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage, Mol Gen Genomics, 277, 427, 10.1007/s00438-006-0199-4 Tanaka, 2011, High-throughput pyrosequencing of the chloroplast genome of a highly neutral-lipid-producing marine pennate diatom, Fistulifera sp. strain JPCC DA0580, Photosynth Res, 109, 223, 10.1007/s11120-011-9622-8 Kroth, 2007, Molecular tools to explore the biology of diatoms, 87 Poulsen, 2006, Molecular genetic manipulation of the diatom Thalassiosira pseudonana (Bacillariophyceae), J Phycol, 42, 1059, 10.1111/j.1529-8817.2006.00269.x Muto, 2013, Establishment of a genetic transformation system for the marine pennate diatom Fistulifera sp. Strain jpcc da0580—a high triglyceride producer, Mar Biotechnol, 15, 48, 10.1007/s10126-012-9457-0 Apt, 1996, Stable nuclear transformation of the diatom Phaeodactylum tricornutum, Mol Gen Genet, 252, 572 Falciatore, 1999, Transformation of nonselectable reporter genes in marine diatoms, Mar Biotechnol, 1, 239, 10.1007/PL00011773 Zhang, 2014, High-efficiency nuclear transformation of the diatom Phaeodactylum tricornutum by electroporation, Mar Genomics, 16, 63, 10.1016/j.margen.2013.10.003 Miyahara, 2013, Highly efficient transformation of the diatom Phaeodactylum tricornutum by multi-pulse electroporation, Biosci Biotechnol Biochem, 77, 874, 10.1271/bbb.120936 Karas, 2015, Designer diatom episomes delivered by bacterial conjugation, Nat Commun, 6, 10.1038/ncomms7925 Chu, 2016, Rapid induction of GFP expression by the nitrate reductase promoter in the diatom Phaeodactylum tricornutum, PeerJ, 4, 10.7717/peerj.2344 Fischer, 1999, Targeting and covalent modification of cell wall and membrane proteins heterologously expressed in the diatom Cylindrotheca fusiformis (Bacillariophyceae), J Phycol, 35, 113, 10.1046/j.1529-8817.1999.3510113.x De Riso, 2009, Gene silencing in the marine diatom Phaeodactylum tricornutum, Nucleic Acids Res, 37, 10.1093/nar/gkp448 Kadono, 2015, Characterization of marine diatom-infecting virus promoters in the model diatom Phaeodactylum tricornutum, Sci Rep, 5, 10.1038/srep18708 Seo, 2015, Development of a new constitutive expression system for the transformation of the diatom Phaeodactylum tricornutum, Algal Res, 11, 50, 10.1016/j.algal.2015.05.012 Zienkiewicz, 2017, Nannochloropsis, a rich source of diacylglycerol acyltransferases for engineering of triacylglycerol content in different hosts, Biotechnol Biofuels, 10, 8, 10.1186/s13068-016-0686-8 Younis, 2014, RNA interference (RNAi) induced gene silencing: a promising approach of hi-tech plant breeding, Int J Biol Sci, 10, 1150, 10.7150/ijbs.10452 Schroda, 2006, RNA silencing in Chlamydomonas: mechanisms and tools, Curr Genet, 49, 69, 10.1007/s00294-005-0042-1 Huang, 2011, Identification and characterization of microRNAs from Phaeodactylum tricornutum by high-throughput sequencing and bioinformatics analysis, BMC Genomics, 12, 337, 10.1186/1471-2164-12-337 Kaur, 2015, Reduction in carotenoid levels in the marine diatom Phaeodactylum tricornutum by artificial micrornas targeted against the endogenous phytoene synthase gene, Mar Biotechnol, 17, 1, 10.1007/s10126-014-9593-9 Shin, 2016, CRISPR/Cas9-induced knockout and knock-in mutations in Chlamydomonas reinhardtii, Sci Rep, 6, 10.1038/srep27810 Wang, 2016, Genome editing of model oleaginous microalgae Nannochloropsis spp. by CRISPR/Cas9, Plant J, 88, 1071, 10.1111/tpj.13307 Nymark, 2016, A CRISPR/Cas9 system adapted for gene editing in marine algae, Sci Rep, 6, 10.1038/srep24951 Hopes, 2016, Editing of the urease gene by CRISPR-Cas in the diatom Thalassiosira pseudonana, Plant Methods, 12, 49, 10.1186/s13007-016-0148-0 Kaufman, 2008, 68 Legendre, 2012 Murtagh, 2014, Ward's hierarchical agglomerative clustering method: Which algorithms implement Ward's criterion?, J Classif, 31, 274, 10.1007/s00357-014-9161-z Kaever, 2009, MarVis: a tool for clustering and visualization of metabolic biomarkers, BMC Bioinform, 10, 92, 10.1186/1471-2105-10-92 Niu, 2016, Molecular characterization of a glycerol-3-phosphate acyltransferase reveals key features essential for triacylglycerol production in Phaeodactylum tricornutum, Biotechnol Biofuels, 9, 1, 10.1186/s13068-016-0478-1 Domergue, 2002, Cloning and functional characterization of Phaeodactylum tricornutum front-end desaturases involved in eicosapentaenoic acid biosynthesis, Eur J Biochem, 269, 4105, 10.1046/j.1432-1033.2002.03104.x Pasquet, 2014, Fatty acids profile and temperature in the cultured marine diatom Odontella aurita, J Appl Phycol, 26, 2265, 10.1007/s10811-014-0252-3 Artamonova, 2017, Lipid content and fatty acid composition of Porosira glacialis and Attheya longicornis in response to carbon dioxide (CO2) aeration, PLoS One, 12, 10.1371/journal.pone.0177703 Li, 2017, Optimization of growth conditions and fatty acid analysis for three freshwater diatom isolates, Phycol Res, 65, 177, 10.1111/pre.12174