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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Veröffentlicht in:PloS one 2013-07, Vol.8 (7), p.e68232-e68232
Hauptverfasser: Kim, Gwang Hoon, Jeong, Hae Jin, Yoo, Yeong Du, Kim, Sunju, Han, Ji Hee, Han, Jong Won, Zuccarello, Giuseppe C
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Jeong, Hae Jin
Yoo, Yeong Du
Kim, Sunju
Han, Ji Hee
Han, Jong Won
Zuccarello, Giuseppe C
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 &lt;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. 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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 &lt;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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