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The zoospores of the thraustochytrid Aurantiochytrium limacinum: Transcriptional reprogramming and lipid metabolism associated to their specific functions
Summary 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 partic...
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Published in: | Environmental microbiology 2020-05, Vol.22 (5), p.1901-1916 |
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creator | Dellero, Younès Maës, Cécile Morabito, Christian Schuler, Martin Bournaud, Caroline Aiese Cigliano, Riccardo Maréchal, Eric Amato, Alberto Rébeillé, Fabrice |
description | Summary
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. |
doi_str_mv | 10.1111/1462-2920.14978 |
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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.</description><identifier>ISSN: 1462-2912</identifier><identifier>EISSN: 1462-2920</identifier><identifier>DOI: 10.1111/1462-2920.14978</identifier><identifier>PMID: 32147875</identifier><language>eng</language><publisher>Hoboken, USA: John Wiley & Sons, Inc</publisher><subject>Amino acids ; Amino Acids - metabolism ; Animals ; Biochemistry, Molecular Biology ; Cell division ; Cell Division - genetics ; Cells ; Computer Simulation ; Culture Media - metabolism ; Decomposers ; Diploids ; Diploidy ; DNA ; Flow cytometry ; Frequency analysis ; Genes ; Glycolysis ; Glycolysis - genetics ; Life cycle ; Life Cycle Stages ; Life cycles ; Life Sciences ; Life span ; Lipase ; Lipid metabolism ; Lipid Metabolism - genetics ; Lipid Metabolism - physiology ; Lipids ; Lipids - analysis ; Mangroves ; Metabolism ; Nucleic acids ; Nucleotide sequence ; Oxidation ; PCR ; Ploidy ; Ribonucleic acid ; RNA ; Signal transduction ; Signal Transduction - genetics ; Spores - growth & development ; Stramenopiles - genetics ; Stramenopiles - metabolism ; Survival ; Transcription ; Transcription, Genetic - genetics ; Zoospores</subject><ispartof>Environmental microbiology, 2020-05, Vol.22 (5), p.1901-1916</ispartof><rights>2020 Society for Applied Microbiology and John Wiley & Sons Ltd.</rights><rights>2020 Society for Applied Microbiology and John Wiley & Sons Ltd</rights><rights>Attribution</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4468-4513c0edc2b06f68c4f1535749484b6c301c65c5636f0bcf63100f65bdcd8a403</citedby><cites>FETCH-LOGICAL-c4468-4513c0edc2b06f68c4f1535749484b6c301c65c5636f0bcf63100f65bdcd8a403</cites><orcidid>0000-0002-3193-7299 ; 0000-0002-9126-5535 ; 0000-0002-0060-1696 ; 0000-0001-6038-8199</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32147875$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02613868$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Dellero, Younès</creatorcontrib><creatorcontrib>Maës, Cécile</creatorcontrib><creatorcontrib>Morabito, Christian</creatorcontrib><creatorcontrib>Schuler, Martin</creatorcontrib><creatorcontrib>Bournaud, Caroline</creatorcontrib><creatorcontrib>Aiese Cigliano, Riccardo</creatorcontrib><creatorcontrib>Maréchal, Eric</creatorcontrib><creatorcontrib>Amato, Alberto</creatorcontrib><creatorcontrib>Rébeillé, Fabrice</creatorcontrib><title>The zoospores of the thraustochytrid Aurantiochytrium limacinum: Transcriptional reprogramming and lipid metabolism associated to their specific functions</title><title>Environmental microbiology</title><addtitle>Environ Microbiol</addtitle><description>Summary
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.</description><subject>Amino acids</subject><subject>Amino Acids - metabolism</subject><subject>Animals</subject><subject>Biochemistry, Molecular Biology</subject><subject>Cell division</subject><subject>Cell Division - genetics</subject><subject>Cells</subject><subject>Computer Simulation</subject><subject>Culture Media - metabolism</subject><subject>Decomposers</subject><subject>Diploids</subject><subject>Diploidy</subject><subject>DNA</subject><subject>Flow cytometry</subject><subject>Frequency analysis</subject><subject>Genes</subject><subject>Glycolysis</subject><subject>Glycolysis - genetics</subject><subject>Life cycle</subject><subject>Life Cycle Stages</subject><subject>Life cycles</subject><subject>Life Sciences</subject><subject>Life span</subject><subject>Lipase</subject><subject>Lipid metabolism</subject><subject>Lipid Metabolism - genetics</subject><subject>Lipid Metabolism - physiology</subject><subject>Lipids</subject><subject>Lipids - analysis</subject><subject>Mangroves</subject><subject>Metabolism</subject><subject>Nucleic acids</subject><subject>Nucleotide sequence</subject><subject>Oxidation</subject><subject>PCR</subject><subject>Ploidy</subject><subject>Ribonucleic acid</subject><subject>RNA</subject><subject>Signal transduction</subject><subject>Signal Transduction - genetics</subject><subject>Spores - growth & development</subject><subject>Stramenopiles - genetics</subject><subject>Stramenopiles - metabolism</subject><subject>Survival</subject><subject>Transcription</subject><subject>Transcription, Genetic - genetics</subject><subject>Zoospores</subject><issn>1462-2912</issn><issn>1462-2920</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><recordid>eNqFkU1v1DAQhi0EoqVw5oYscSmHbe34Iwm3VVVopUVclrPlOHbXVRwHf4C2P6W_tk6z7IFLfbFn5pnXHr8AfMToApd1iSmvVlVblZC2dfMKnB4zr49nXJ2AdzHeI4RrUqO34IRUmNZNzU7B43an4YP3cfJBR-gNTCWRdkHmmLza7VOwPVznIMdkD3F2cLBOKjtm9xVuSymqYKdSH-UAg56CvwvSOTveQTn2BZ6KhtNJdn6w0UEZo1dWJt3D5OcLbYBx0soaq6DJo5ql4nvwxsgh6g-H_Qz8-na9vbpZbX5-v71ab1aKUt6sKMNEId2rqkPc8EZRgxlhNW1pQzuuCMKKM8U44QZ1ynCCETKcdb3qG0kROQNfFt2dHMQUymRhL7y04ma9EXMOVRyThjd_cGHPF7bM-DvrmISzUelhkKP2OYqK1IyhljzLfv4Pvfc5lB-aqbamHHHWFOpyoVTwMQZtji_ASMwWi9lEMRsqni0uHZ8Ourlzuj_y_zwtAFuAv3bQ-5f0xPWP20X4CXjksvY</recordid><startdate>202005</startdate><enddate>202005</enddate><creator>Dellero, Younès</creator><creator>Maës, Cécile</creator><creator>Morabito, Christian</creator><creator>Schuler, Martin</creator><creator>Bournaud, Caroline</creator><creator>Aiese Cigliano, Riccardo</creator><creator>Maréchal, Eric</creator><creator>Amato, Alberto</creator><creator>Rébeillé, Fabrice</creator><general>John Wiley & Sons, Inc</general><general>Wiley Subscription Services, Inc</general><general>Society for Applied Microbiology and Wiley-Blackwell</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QH</scope><scope>7QL</scope><scope>7ST</scope><scope>7T7</scope><scope>7TN</scope><scope>7U9</scope><scope>7UA</scope><scope>8FD</scope><scope>C1K</scope><scope>F1W</scope><scope>FR3</scope><scope>H94</scope><scope>H95</scope><scope>H97</scope><scope>L.G</scope><scope>M7N</scope><scope>P64</scope><scope>SOI</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><orcidid>https://orcid.org/0000-0002-3193-7299</orcidid><orcidid>https://orcid.org/0000-0002-9126-5535</orcidid><orcidid>https://orcid.org/0000-0002-0060-1696</orcidid><orcidid>https://orcid.org/0000-0001-6038-8199</orcidid></search><sort><creationdate>202005</creationdate><title>The zoospores of the thraustochytrid Aurantiochytrium limacinum: Transcriptional reprogramming and lipid metabolism associated to their specific functions</title><author>Dellero, Younès ; 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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.</abstract><cop>Hoboken, USA</cop><pub>John Wiley & Sons, Inc</pub><pmid>32147875</pmid><doi>10.1111/1462-2920.14978</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-3193-7299</orcidid><orcidid>https://orcid.org/0000-0002-9126-5535</orcidid><orcidid>https://orcid.org/0000-0002-0060-1696</orcidid><orcidid>https://orcid.org/0000-0001-6038-8199</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Amino acids Amino Acids - metabolism Animals Biochemistry, Molecular Biology Cell division Cell Division - genetics Cells Computer Simulation Culture Media - metabolism Decomposers Diploids Diploidy DNA Flow cytometry Frequency analysis Genes Glycolysis Glycolysis - genetics Life cycle Life Cycle Stages Life cycles Life Sciences Life span Lipase Lipid metabolism Lipid Metabolism - genetics Lipid Metabolism - physiology Lipids Lipids - analysis Mangroves Metabolism Nucleic acids Nucleotide sequence Oxidation PCR Ploidy Ribonucleic acid RNA Signal transduction Signal Transduction - genetics Spores - growth & development Stramenopiles - genetics Stramenopiles - metabolism Survival Transcription Transcription, Genetic - genetics Zoospores |
title | The zoospores of the thraustochytrid Aurantiochytrium limacinum: Transcriptional reprogramming and lipid metabolism associated to their specific functions |
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