Still acting green: continued expression of photosynthetic genes in the heterotrophic Dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata)
The loss of photosynthetic function should lead to the cessation of expression and finally loss of photosynthetic genes in the new heterotroph. Dinoflagellates are known to have lost their photosynthetic ability several times. Dinoflagellates have also acquired photosynthesis from other organisms, e...
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description | The loss of photosynthetic function should lead to the cessation of expression and finally loss of photosynthetic genes in the new heterotroph. Dinoflagellates are known to have lost their photosynthetic ability several times. Dinoflagellates have also acquired photosynthesis from other organisms, either on a long-term basis or as "kleptoplastids" multiple times. The fate of photosynthetic gene expression in heterotrophs can be informative into evolution of gene expression patterns after functional loss, and the dinoflagellates ability to acquire new photosynthetic function through additional endosymbiosis. To explore this we analyzed a large-scale EST database consisting of 151,091 unique sequences (29,170 contigs, 120,921 singletons) obtained from 454 pyrosequencing of the heterotrophic dinoflagellate Pfiesteria piscicida. About 597 contigs from P. piscicida showed significant homology (E-value |
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Dinoflagellates are known to have lost their photosynthetic ability several times. Dinoflagellates have also acquired photosynthesis from other organisms, either on a long-term basis or as "kleptoplastids" multiple times. The fate of photosynthetic gene expression in heterotrophs can be informative into evolution of gene expression patterns after functional loss, and the dinoflagellates ability to acquire new photosynthetic function through additional endosymbiosis. To explore this we analyzed a large-scale EST database consisting of 151,091 unique sequences (29,170 contigs, 120,921 singletons) obtained from 454 pyrosequencing of the heterotrophic dinoflagellate Pfiesteria piscicida. About 597 contigs from P. piscicida showed significant homology (E-value <e(-30)) with proteins associated with plastid and photosynthetic function. Most of the genes involved in the Calvin-Benson cycle were found, genes of the light-dependent reaction were also identified. Also genes of associated pathways including the chorismate pathway and genes involved in starch metabolism were discovered. BLAST searches and phylogenetic analysis suggest that these plastid-associated genes originated from several different photosynthetic ancestors. The Calvin-Benson cycle genes are mostly associated with genes derived from the secondary plastids of peridinin-containing dinoflagellates, while the light-harvesting genes are derived from diatoms, or diatoms that are tertiary plastids in other dinoflagellates. The continued expression of many genes involved in photosynthetic pathways indicates that the loss of transcriptional regulation may occur well after plastid loss and could explain the organism's ability to "capture" new plastids (i.e. different secondary endosymbiosis or tertiary symbioses) to renew photosynthetic function.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0068232</identifier><identifier>PMID: 23874554</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Alveolata ; Bacillariophyceae ; Bioinformatics ; Biology ; Carbohydrate metabolism ; Carbon ; Cladistic analysis ; Computational Biology ; Databases, Genetic ; Dinoflagellates ; Dinoflagellida - genetics ; Dinophyceae ; Environmental science ; Evolution ; Gene expression ; Gene regulation ; Genes ; Genomes ; Heterotrophs ; Homology ; Light ; Metabolism ; Microorganisms ; Parasites ; Pathways ; Peridiniales ; Pfiesteria piscicida ; Photosynthesis ; Photosynthesis - genetics ; Photosynthesis - physiology ; Phylogenetics ; Phylogeny ; Plant biochemistry ; Plastids ; Proteins ; Pyrrophycophyta ; Starch ; Symbiosis ; Transcription ; Transcription (Genetics)</subject><ispartof>PloS one, 2013-07, Vol.8 (7), p.e68232-e68232</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Kim et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2013 Kim et al 2013 Kim et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c791t-ba8d3537ee45f3f7ee7c915fa80a28abd7712a8277d25c8f07ce979459f673233</citedby><cites>FETCH-LOGICAL-c791t-ba8d3537ee45f3f7ee7c915fa80a28abd7712a8277d25c8f07ce979459f673233</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3712967/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3712967/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,864,885,2102,2928,23866,27924,27925,53791,53793,79600,79601</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23874554$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><contributor>Prigent, Claude</contributor><creatorcontrib>Kim, Gwang Hoon</creatorcontrib><creatorcontrib>Jeong, Hae Jin</creatorcontrib><creatorcontrib>Yoo, Yeong Du</creatorcontrib><creatorcontrib>Kim, Sunju</creatorcontrib><creatorcontrib>Han, Ji Hee</creatorcontrib><creatorcontrib>Han, Jong Won</creatorcontrib><creatorcontrib>Zuccarello, Giuseppe C</creatorcontrib><title>Still acting green: continued expression of photosynthetic genes in the heterotrophic Dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata)</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>The loss of photosynthetic function should lead to the cessation of expression and finally loss of photosynthetic genes in the new heterotroph. Dinoflagellates are known to have lost their photosynthetic ability several times. Dinoflagellates have also acquired photosynthesis from other organisms, either on a long-term basis or as "kleptoplastids" multiple times. The fate of photosynthetic gene expression in heterotrophs can be informative into evolution of gene expression patterns after functional loss, and the dinoflagellates ability to acquire new photosynthetic function through additional endosymbiosis. To explore this we analyzed a large-scale EST database consisting of 151,091 unique sequences (29,170 contigs, 120,921 singletons) obtained from 454 pyrosequencing of the heterotrophic dinoflagellate Pfiesteria piscicida. About 597 contigs from P. piscicida showed significant homology (E-value <e(-30)) with proteins associated with plastid and photosynthetic function. Most of the genes involved in the Calvin-Benson cycle were found, genes of the light-dependent reaction were also identified. Also genes of associated pathways including the chorismate pathway and genes involved in starch metabolism were discovered. BLAST searches and phylogenetic analysis suggest that these plastid-associated genes originated from several different photosynthetic ancestors. The Calvin-Benson cycle genes are mostly associated with genes derived from the secondary plastids of peridinin-containing dinoflagellates, while the light-harvesting genes are derived from diatoms, or diatoms that are tertiary plastids in other dinoflagellates. The continued expression of many genes involved in photosynthetic pathways indicates that the loss of transcriptional regulation may occur well after plastid loss and could explain the organism's ability to "capture" new plastids (i.e. different secondary endosymbiosis or tertiary symbioses) to renew photosynthetic function.</description><subject>Alveolata</subject><subject>Bacillariophyceae</subject><subject>Bioinformatics</subject><subject>Biology</subject><subject>Carbohydrate metabolism</subject><subject>Carbon</subject><subject>Cladistic analysis</subject><subject>Computational Biology</subject><subject>Databases, Genetic</subject><subject>Dinoflagellates</subject><subject>Dinoflagellida - genetics</subject><subject>Dinophyceae</subject><subject>Environmental science</subject><subject>Evolution</subject><subject>Gene expression</subject><subject>Gene regulation</subject><subject>Genes</subject><subject>Genomes</subject><subject>Heterotrophs</subject><subject>Homology</subject><subject>Light</subject><subject>Metabolism</subject><subject>Microorganisms</subject><subject>Parasites</subject><subject>Pathways</subject><subject>Peridiniales</subject><subject>Pfiesteria piscicida</subject><subject>Photosynthesis</subject><subject>Photosynthesis - genetics</subject><subject>Photosynthesis - physiology</subject><subject>Phylogenetics</subject><subject>Phylogeny</subject><subject>Plant biochemistry</subject><subject>Plastids</subject><subject>Proteins</subject><subject>Pyrrophycophyta</subject><subject>Starch</subject><subject>Symbiosis</subject><subject>Transcription</subject><subject>Transcription (Genetics)</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><sourceid>DOA</sourceid><recordid>eNqNk99u0zAUxiMEYqPwBggsIaFNoiW2k9jmAmka_ypN2sSAW8t1jlNPrh3sZNqegxfGpd20ol1MuXB8zu98cb7jUxQvcTnDlOH3F2GMXrlZHzzMyrLhhJJHxT4WlEwbUtLHd973imcpXZRlTXnTPC32COWsqutqv_hzPljnkNKD9R3qIoD_gHTweTtCi-Cqj5CSDR4Fg_plGEK69sMSBqtRBx4Ssh7lPcohiGGIoV_m1Cfrg3GqA-fUAOjMWEg5bxXqbdJW21ahg7McaK23ykF6h47cJYRMq8PnxROjXIIX23VS_Pzy-cfxt-nJ6df58dHJVDOBh-lC8ZbWlAFUtaEmr0wLXBvFS0W4WrSMYaI4YawlteamZBoEE1UtTMMooXRSvN7o9i4kufUzSVwRRhkRvMnEfEO0QV3IPtqVitcyKCv_BULspIrZCgcS1yLrloK0C1OxSiyw4lhjQhbckNborPVx-7VxsYJWgx-icjuiuxlvl7ILlzI3m4h84klxsBWI4feY_ZSr7OXaYQ9hXJ-blrzGjOAHoBg3NP8nyeib_9D7jdhSXW6WtN7kTiu9FpVHFeOkrgURmZrdQ-WnhZXNlwqMzfGdgsOdgvXFg6uhU2NKcn7-_eHs6a9d9u0ddgnKDcsU3Djki5x2wWoD6hhSimBu-4FLuR6zGzfkeszkdsxy2au7vbwtupkr-hfI3iS2</recordid><startdate>20130716</startdate><enddate>20130716</enddate><creator>Kim, Gwang Hoon</creator><creator>Jeong, Hae Jin</creator><creator>Yoo, Yeong Du</creator><creator>Kim, Sunju</creator><creator>Han, Ji Hee</creator><creator>Han, Jong Won</creator><creator>Zuccarello, Giuseppe C</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</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>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>7X8</scope><scope>F1W</scope><scope>H95</scope><scope>L.G</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130716</creationdate><title>Still acting green: continued expression of photosynthetic genes in the heterotrophic Dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata)</title><author>Kim, Gwang Hoon ; Jeong, Hae Jin ; Yoo, Yeong Du ; Kim, Sunju ; Han, Ji Hee ; Han, Jong Won ; Zuccarello, Giuseppe C</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c791t-ba8d3537ee45f3f7ee7c915fa80a28abd7712a8277d25c8f07ce979459f673233</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Alveolata</topic><topic>Bacillariophyceae</topic><topic>Bioinformatics</topic><topic>Biology</topic><topic>Carbohydrate metabolism</topic><topic>Carbon</topic><topic>Cladistic analysis</topic><topic>Computational Biology</topic><topic>Databases, Genetic</topic><topic>Dinoflagellates</topic><topic>Dinoflagellida - genetics</topic><topic>Dinophyceae</topic><topic>Environmental science</topic><topic>Evolution</topic><topic>Gene expression</topic><topic>Gene regulation</topic><topic>Genes</topic><topic>Genomes</topic><topic>Heterotrophs</topic><topic>Homology</topic><topic>Light</topic><topic>Metabolism</topic><topic>Microorganisms</topic><topic>Parasites</topic><topic>Pathways</topic><topic>Peridiniales</topic><topic>Pfiesteria piscicida</topic><topic>Photosynthesis</topic><topic>Photosynthesis - genetics</topic><topic>Photosynthesis - physiology</topic><topic>Phylogenetics</topic><topic>Phylogeny</topic><topic>Plant biochemistry</topic><topic>Plastids</topic><topic>Proteins</topic><topic>Pyrrophycophyta</topic><topic>Starch</topic><topic>Symbiosis</topic><topic>Transcription</topic><topic>Transcription (Genetics)</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Kim, Gwang Hoon</creatorcontrib><creatorcontrib>Jeong, Hae Jin</creatorcontrib><creatorcontrib>Yoo, Yeong Du</creatorcontrib><creatorcontrib>Kim, Sunju</creatorcontrib><creatorcontrib>Han, Ji Hee</creatorcontrib><creatorcontrib>Han, Jong Won</creatorcontrib><creatorcontrib>Zuccarello, Giuseppe C</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Dinoflagellates are known to have lost their photosynthetic ability several times. Dinoflagellates have also acquired photosynthesis from other organisms, either on a long-term basis or as "kleptoplastids" multiple times. The fate of photosynthetic gene expression in heterotrophs can be informative into evolution of gene expression patterns after functional loss, and the dinoflagellates ability to acquire new photosynthetic function through additional endosymbiosis. To explore this we analyzed a large-scale EST database consisting of 151,091 unique sequences (29,170 contigs, 120,921 singletons) obtained from 454 pyrosequencing of the heterotrophic dinoflagellate Pfiesteria piscicida. About 597 contigs from P. piscicida showed significant homology (E-value <e(-30)) with proteins associated with plastid and photosynthetic function. Most of the genes involved in the Calvin-Benson cycle were found, genes of the light-dependent reaction were also identified. Also genes of associated pathways including the chorismate pathway and genes involved in starch metabolism were discovered. BLAST searches and phylogenetic analysis suggest that these plastid-associated genes originated from several different photosynthetic ancestors. The Calvin-Benson cycle genes are mostly associated with genes derived from the secondary plastids of peridinin-containing dinoflagellates, while the light-harvesting genes are derived from diatoms, or diatoms that are tertiary plastids in other dinoflagellates. The continued expression of many genes involved in photosynthetic pathways indicates that the loss of transcriptional regulation may occur well after plastid loss and could explain the organism's ability to "capture" new plastids (i.e. different secondary endosymbiosis or tertiary symbioses) to renew photosynthetic function.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23874554</pmid><doi>10.1371/journal.pone.0068232</doi><tpages>e68232</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Alveolata Bacillariophyceae Bioinformatics Biology Carbohydrate metabolism Carbon Cladistic analysis Computational Biology Databases, Genetic Dinoflagellates Dinoflagellida - genetics Dinophyceae Environmental science Evolution Gene expression Gene regulation Genes Genomes Heterotrophs Homology Light Metabolism Microorganisms Parasites Pathways Peridiniales Pfiesteria piscicida Photosynthesis Photosynthesis - genetics Photosynthesis - physiology Phylogenetics Phylogeny Plant biochemistry Plastids Proteins Pyrrophycophyta Starch Symbiosis Transcription Transcription (Genetics) |
title | Still acting green: continued expression of photosynthetic genes in the heterotrophic Dinoflagellate Pfiesteria piscicida (Peridiniales, Alveolata) |
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