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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. Proposal of a new thraustochytrid genus Hondaea gen. nov. and comparison of its lipid dynamics with the closely related pseudo-cryptic genus Aurantiochytrium

Author

Juliette Jouhet, Fabrice Rébeillé, Mathilde Cussac, Christian Morabito, Eric Maréchal, Younès Dellero, Riccardo Aiese Cigliano, Alberto Amato, Khawla Seddiki, Walter Sanseverino, Josselin Lupette, Olivier Cagnac, Suzanne Rose, Marcel Kuntz, 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), Fermentalg, Sequentia Biotech SL, Trans'Alg Bpifrance project, Fermentalg-CEA partnership, ANR-11-BTBR-0008/11-BTBR-0008,OCEANOMICS,Biotechnologies et bioressources pour la valorisation des écosystèmes marins planctoniques(2011), ANR–10–LABEX–04 ,GRAL,Labex, 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), ANR-11-BTBR-0008,OCEANOMICS,Biotechnologies et bioressources pour la valorisation des écosystèmes marins planctoniques(2011), ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010), Physiologie cellulaire et végétale [2016-2019] (LPCV [2016-2019]), Fermentalg SA, UMR 1417 PCV Laboratoire de Physiologie Cellulaire Végétale. Centre de recherche Auvergne-Rhône-Alpes, Institut National de la Recherche Agronomique (INRA), Oceanomics ANR program 11-BTBR-0008, French National Research Agency ANR-10-LABEX-04 ANR-11-BTBR-0008, and PhD Flagship program of CEA high commissioner

Subjects
0106 biological sciences, 0301 basic medicine, Canthaxanthin, [SDV.BIO]Life Sciences [q-bio]/Biotechnology, [SDV]Life Sciences [q-bio], omega 3 fatty acid, Biology, 01 natural sciences, DNA sequencing, 03 medical and health sciences, Genus, 010608 biotechnology, Botany, [SDV.BV]Life Sciences [q-bio]/Vegetal Biology, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, 14. Life underwater, Mangrove, Clade, Gene, Carotenoid, ComputingMilieux_MISCELLANEOUS, Phylogeny, Sterol, chemistry.chemical_classification, Phylogenetic tree, Protist, Fatty acid, 15. Life on land, Mayotte Island, Lipids, Chemotaxonomy, Thraustochytrid, Biotechnological Potential, 030104 developmental biology, Pigment, chemistry, Omega 3, Auriantiochytrium, Sterol-thraustochytrid-triacylglycerol, Agronomy and Crop Science
Abstract

International audience; Thraustochytrids are marine protists highly ecologically relevant in mangrove environments. The family Thraustochytriaceae underwent profound taxonomical rearrangements in the last decade, with the description and emendation of several genera. Here, we identified two new thraustochytrid strains (CCAP 4062/1 and CCAP 4062/3) collected from the same mangrove environment in Mayotte Island (Indian Ocean) and representative of two sister clades in the phylogenetic Aurantiochytrium super Glade. Phylogenomic (on 2389 genes) and phylogenetic analyses on 18S rDNA sequences led us to propose the description of a new genus, Hondaea gen. nov. (CCAP 4062/3), closely related and pseudo-cryptic to Aurantiochytrium (CCAP 4062/1). Compared to Aurantiochytrium, Hondaea did not produce amoeboid cells and its zoospores were smaller. Chemotaxonomical traits, such as fatty acid, sterol, and carotenoid profiles measured along the growth curves, validated the new genus description. Genome sequencing and manual annotation of lipid metabolism genes revealed similar pathways in both strains. However, such pathways showed different dynamics during the growth phases. Aurantiochytrium accumulated carotenoids (canthaxanthin) and large amounts of triacylglycerols enriched in omega 3-docosahexaenoic acid in the stationary phase, while squalene and free cholesterol increased during the early exponential phase. In contrast, Hondaea accumulated low amounts of triacylglycerols enriched in odd and saturated fatty acids during the early exponential phase, whereas free-sterol and carotenoid contents were little affected. These results suggest that these genera evolved independently, although phylogenetically and ecologically closely related. This comparative study also showed that the biotechnological potential of thraus-tochytrids cannot be deduced solely from phylogenetic and genomic analyses.

Published
2018
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