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1. The zoospores of the thraustochytridAurantiochytrium limacinum: Transcriptional reprogramming and lipid metabolism associated to their specific functions

Author

Caroline Bournaud, Cécile Maës, Riccardo Aiese Cigliano, Alberto Amato, Eric Maréchal, Fabrice Rébeillé, Martin Schuler, Christian Morabito, Younès Dellero, LIPID, Physiologie cellulaire et végétale (LPCV), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA), Sequentia Biotech SL, Trans’Alg Bpifrance PSPC partnership, ANR-10-LABX-0049,GRAL,Grenoble Alliance for Integrated Structural Cell Biology(2010), ANR-11-BTBR-0008,OCEANOMICS,Biotechnologies et bioressources pour la valorisation des écosystèmes marins planctoniques(2011), ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017), Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), and Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)

Subjects
Spores, Transcription, Genetic, Cell division, PUFA synthase, Zoospore, Population, RNA-sequencing, ω3-docosahexaenoic acid, Biology, Microbiology, 03 medical and health sciences, Animals, Computer Simulation, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Amino Acids, Fatty acids, education, Gene, Ecology, Evolution, Behavior and Systematics, 030304 developmental biology, Docosahexaenoic Acid, algae, chemistry.chemical_classification, Life Cycle Stages, 0303 health sciences, education.field_of_study, 030306 microbiology, Thraustochytrids, RNA sequencing, Lipid metabolism, Zoospores, 15. Life on land, Peroxisome, biology.organism_classification, Diploidy, Lipids, Culture Media, Amino acid, Cell biology, chemistry, Labyrinthulomycetes, Glycolysis, Cell Division, Stramenopiles, Signal Transduction
Abstract

International audience; Aurantiochytrium limacinum (Thraustochytriaceae, class Labyrinthulomycetes) is a marine Stramenopile and a pioneering mangrove decomposer. Its life cycle involves a non-motile stage and zoospore production. We observed that the composition of the medium, the presence of amino acids in particular, affects the release of zoospores. Two opposite conditions were defined, one with a cell population mainly composed of zoospores and another one with almost only non-motile cells. In silico allelic frequency analysis and flow cytometry suggest that zoospores and non-motile cells share the same ploidy level and are diploid. Through an RNA-seq approach, the transcriptional reprogramming accompanying the formation of zoospores was investigated, with a particular focus on their lipid metabolism. Based on a differential expression analysis, zoospores are characterized by high motility, very active signal transduction, an arrest of the cell division, a low amino acid metabolism and low glycolysis. Focusing on lipid metabolism, genes involved in lipase activities and peroxisomal β-oxidation are upregulated. qRT-PCR of selected lipid genes and lipid analyses during the life span of zoospores confirmed these observations. These results highlight the importance of the lipid dynamics in zoospores and show the metabolic processes required to use these energy-dense molecules as fuel for zoospore survival during their quest of new territories.

Published
2020
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2. An Oil Hyper-Accumulator Mutant Highlights Peroxisomal ATP Import as a Regulatory Step for Fatty Acid Metabolism in Aurantiochytrium limacinum

Author

Gregory Si Larbi, Eric Maréchal, Morgane Michaud, Juliette Jouhet, Martin Schuler, Younès Dellero, Riccardo Aiese Cigliano, Alberto Amato, Denis Falconet, Etienne Deragon, Fabrice Rébeillé, LIPID, Physiologie cellulaire et végétale (LPCV), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA), Sequentia Biotech SL, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Trans’Alg Bpifrance PSPC partnership, ANR-10-LABX-0049,GRAL,Grenoble Alliance for Integrated Structural Cell Biology(2010), ANR-11-BTBR-0008,OCEANOMICS,Biotechnologies et bioressources pour la valorisation des écosystèmes marins planctoniques(2011), ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017), Université de Rennes (UR)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-INSTITUT AGRO Agrocampus Ouest, and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)

Subjects
0106 biological sciences, thraustochytrids, QH301-705.5, Adenylate kinase, 01 natural sciences, 03 medical and health sciences, chemistry.chemical_compound, lipid metabolism, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Biology (General), Gene, triacylglycerol (TAG), 030304 developmental biology, chemistry.chemical_classification, 0303 health sciences, Fatty acid metabolism, Catabolism, Chemistry, General Medicine, Peroxisome, peroxisomal adenylate transporter, Yeast, Complementation, Biochemistry, [SDE]Environmental Sciences, β-oxidation, ω3-docosahexaenoic acid (DHA), 010606 plant biology & botany, Polyunsaturated fatty acid
Abstract

International audience; Thraustochytrids are marine protists that naturally accumulate triacylglycerol with long chains of polyunsaturated fatty acids, such as ω3-docosahexaenoic acid (DHA). They represent a sustainable response to the increasing demand for these "essential" fatty acids (FAs). Following an attempt to transform a strain of Aurantiochytrium limacinum, we serendipitously isolated a clone that did not incorporate any recombinant DNA but contained two to three times more DHA than the original strain. Metabolic analyses indicated a deficit in FA catabolism. However, whole transcriptome analysis did not show down-regulation of genes involved in FA catabolism. Genome sequencing revealed extensive DNA deletion in one allele encoding a putative peroxisomal adenylate transporter. Phylogenetic analyses and yeast complementation experiments confirmed the gene as a peroxisomal adenylate nucleotide transporter (AlANT1), homologous to yeast ScANT1 and plant peroxisomal adenylate nucleotide carrier AtPNC genes. In yeast and plants, a deletion of the peroxisomal adenylate transporter inhibits FA breakdown and induces FA accumulation, a phenotype similar to that described here. In response to this metabolic event, several compensatory mechanisms were observed. In particular, genes involved in FA biosynthesis were upregulated, also contributing to the high FA accumulation. These results support AlANT1 as a promising target for enhancing DHA production in Thraustochytrids.

Published
2021
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3. Illumina and PacBio DNA sequencing data, de novo assembly and annotation of the genome of Aurantiochytrium limacinum strain CCAP_4062/1

Author

Riccardo Aiese Cigliano, Alberto Amato, Christian Morabito, Eric Maréchal, Fabrice Rébeillé, LIPID, Physiologie cellulaire et végétale (LPCV), Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Sequentia Biotech SL, Trans’Alg Bpifrance PSPC partnership, ANR-10-LABX-0049,GRAL,Labex GRAL(2010), ANR-11-BTBR-0008,OCEANOMICS,Biotechnologies et bioressources pour la valorisation des écosystèmes marins planctoniques(2011), ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA), and ANR-10-LABX-0049,GRAL,Grenoble Alliance for Integrated Structural Cell Biology(2010)

Subjects
[SDV]Life Sciences [q-bio], Sequence assembly, Genomics, Computational biology, Biology, lcsh:Computer applications to medicine. Medical informatics, Genome, DNA sequencing, 03 medical and health sciences, Annotation, 0302 clinical medicine, Next generation sequencing, lcsh:Science (General), ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, 0303 health sciences, Multidisciplinary, Strain (biology), Genome project, Thraustochytrid, lcsh:R858-859.7, Structural annotation, Third generation sequencing, 030217 neurology & neurosurgery, Reference genome, Biotechnology, lcsh:Q1-390
Abstract

The complete genome of the thraustochytrid Aurantiochytrium limacinum strain CCAP_4062/1 was sequenced using both Illumina Novaseq 6000 and third generation sequencing technology PacBio RSII in order to obtain trustworthy assembly and annotation. The reads from both platforms were combined at multiple levels in order to obtain a reliable assembly, then compared to the A. limacinum ATCCⓇ MYA1381™ reference genome. The final assembly was annotated with the help of strain CCAP_4062/1 RNAseq data. A. limacinum strain CCAP_4062/1 is an industrial strain used for the production of very long chain polyunsaturated fatty acids, like the docosahexaenoic acid that is an essential fatty acid synthesised only at very low pace in humans and vertebrates . Thraustochytrids in general and Aurantiochytrium more specifically, are used for carotenoid and squalene production as well. Beside their biotechnological interest, thraustochytrids play a crucial role in both inshore and oceanic basins ecosystems. Genome sequences will foster biotechnological as well as ecological studies.

Published
2020
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4. The lipid metabolism in thraustochytrids

Author

Fabrice Rébeillé, Eric Maréchal, Martin Schuler, Christian Morabito, Younès Dellero, Caroline Bournaud, Riccardo Aiese Cigliano, Alberto Amato, Cécile Maës, LIPID, Physiologie cellulaire et végétale (LPCV), Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes (UGA)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Sequentia Biotech SL, Institut de Génétique, Environnement et Protection des Plantes (IGEPP), AGROCAMPUS OUEST-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National de la Recherche Agronomique (INRA), Trans'Alg Bpifrance PSPC Partnership, ANR–10–LABEX–04 ,GRAL,Labex, ANR-11-BTBR-0008/11-BTBR-0008,OCEANOMICS,Biotechnologies et bioressources pour la valorisation des écosystèmes marins planctoniques(2011), ANR-17-EURE-0003,University Grenoble Alpes graduate school, Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes [2016-2019] (UGA [2016-2019])-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes [2016-2019] (UGA [2016-2019])-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Institut National de la Recherche Agronomique (INRA)-Université de Rennes (UR)-AGROCAMPUS OUEST, ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010), ANR-11-BTBR-0008,OCEANOMICS,Biotechnologies et bioressources pour la valorisation des écosystèmes marins planctoniques(2011), ANR-17-EURE-0003,CBH-EUR-GS,CBH-EUR-GS(2017), Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Université Grenoble Alpes (UGA), Institut National de la Recherche Agronomique (INRA)-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-AGROCAMPUS OUEST, and Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)

Subjects
0106 biological sciences, 0301 basic medicine, Ecophysiology, Squalene, [SDV.BIO]Life Sciences [q-bio]/Biotechnology, PUFA synthase, Heterotroph, Biology, 01 natural sciences, Biochemistry, [SDV.MP.PRO]Life Sciences [q-bio]/Microbiology and Parasitology/Protistology, 03 medical and health sciences, Botany, Animals, 14. Life underwater, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biochemistry [q-bio.BM], Triacylglycerol (TAG), Carotenoid, ComputingMilieux_MISCELLANEOUS, chemistry.chemical_classification, Nitrogen deficiency, Thraustochytrids, Fatty acid, Lipid metabolism, Cell Biology, Metabolism, Lipids, Carotenoids, Food web, [SDV.BBM.BC]Life Sciences [q-bio]/Biochemistry, Molecular Biology/Biomolecules [q-bio.BM], Fatty acid synthase, 030104 developmental biology, chemistry, biology.protein, ω3-docosahexaenoic acid (DHA), Stramenopiles, 010606 plant biology & botany
Abstract

International audience; Thraustochytrids are unicellular heterotrophic marine protists of the Stramenopile group, often considered as non-photosynthetic microalgae. They have been isolated from a wide range of habitats including deep sea, but are mostly present in waters rich in sediments and organic materials. They are abundant in mangrove forests where they are major colonizers, feeding on decaying leaves and initiating the mangrove food web. Discovered 80 years ago, they have recently attracted considerable attention due to their biotechnological potential. This interest arises from their fast growth, their specific lipid metabolism and the improvement of the genetic tools and transformation techniques. These organisms are particularly rich in omega 3-docosahexaenoic acid (DHA), an 'essential' fatty acid poorly encountered in land plants and animals but required for human health. To produce their DHA, thraustochytrids use a sophisticated system different from the classical fatty acid synthase system. They are also a potential source of squalene and carotenoids. Here we review our current knowledge about the life cycle, ecophysiology, and metabolism of these organisms, with a particular focus on lipid dynamics. We describe the different pathways involved in lipid and fatty acid syntheses, emphasizing their specificity, and we report on the recent efforts aimed to engineer their lipid metabolism.

Published
2019
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