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The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles

BACKGROUND: Haptophytes are widely and abundantly distributed in both marine and freshwater ecosystems. Few genomic analyses of representatives within this taxon have been reported, despite their early evolutionary origins and their prominent role in global carbon fixation. RESULTS: The complete mit...

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Autores principales: Hovde, Blake T, Starkenburg, Shawn R, Hunsperger, Heather M, Mercer, Laina D, Deodato, Chloe R, Jha, Ramesh K, Chertkov, Olga, Monnat, Raymond J, Cattolico, Rose Ann
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4226036/
https://www.ncbi.nlm.nih.gov/pubmed/25034814
http://dx.doi.org/10.1186/1471-2164-15-604
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author Hovde, Blake T
Starkenburg, Shawn R
Hunsperger, Heather M
Mercer, Laina D
Deodato, Chloe R
Jha, Ramesh K
Chertkov, Olga
Monnat, Raymond J
Cattolico, Rose Ann
author_facet Hovde, Blake T
Starkenburg, Shawn R
Hunsperger, Heather M
Mercer, Laina D
Deodato, Chloe R
Jha, Ramesh K
Chertkov, Olga
Monnat, Raymond J
Cattolico, Rose Ann
author_sort Hovde, Blake T
collection PubMed
description BACKGROUND: Haptophytes are widely and abundantly distributed in both marine and freshwater ecosystems. Few genomic analyses of representatives within this taxon have been reported, despite their early evolutionary origins and their prominent role in global carbon fixation. RESULTS: The complete mitochondrial and chloroplast genome sequences of the haptophyte Chrysochromulina tobin (Prymnesiales) provide insight into the architecture and gene content of haptophyte organellar genomes. The mitochondrial genome (~34 kb) encodes 21 protein coding genes and contains a complex, 9 kb tandem repeat region. Similar to other haptophytes and rhodophytes, but not cryptophytes or stramenopiles, the mitochondrial genome has lost the nad7, nad9 and nad11 genes. The ~105 kb chloroplast genome encodes 112 protein coding genes, including ycf39 which has strong structural homology to NADP-binding nitrate transcriptional regulators; a divergent ‘CheY-like’ two-component response regulator (ycf55) and Tic/Toc (ycf60 and ycf80) membrane transporters. Notably, a zinc finger domain has been identified in the rpl36 ribosomal protein gene of all chloroplasts sequenced to date with the exception of haptophytes and cryptophytes - algae that have gained (via lateral gene transfer) an alternative rpl36 lacking the zinc finger motif. The two C. tobin chloroplast ribosomal RNA operon spacer regions differ in tRNA content. Additionally, each ribosomal operon contains multiple single nucleotide polymorphisms (SNPs) - a pattern observed in rhodophytes and cryptophytes, but few stramenopiles. Analysis of small (<200 bp) chloroplast encoded tandem and inverted repeats in C. tobin and 78 other algal chloroplast genomes show that repeat type, size and location are correlated with gene identity and taxonomic clade. CONCLUSION: The Chrysochromulina tobin organellar genomes provide new insight into organellar function and evolution. These are the first organellar genomes to be determined for the prymnesiales, a taxon that is present in both oceanic and freshwater systems and represents major primary photosynthetic producers and contributors to global ecosystem stability. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-604) contains supplementary material, which is available to authorized users.
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spelling pubmed-42260362014-11-11 The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles Hovde, Blake T Starkenburg, Shawn R Hunsperger, Heather M Mercer, Laina D Deodato, Chloe R Jha, Ramesh K Chertkov, Olga Monnat, Raymond J Cattolico, Rose Ann BMC Genomics Research Article BACKGROUND: Haptophytes are widely and abundantly distributed in both marine and freshwater ecosystems. Few genomic analyses of representatives within this taxon have been reported, despite their early evolutionary origins and their prominent role in global carbon fixation. RESULTS: The complete mitochondrial and chloroplast genome sequences of the haptophyte Chrysochromulina tobin (Prymnesiales) provide insight into the architecture and gene content of haptophyte organellar genomes. The mitochondrial genome (~34 kb) encodes 21 protein coding genes and contains a complex, 9 kb tandem repeat region. Similar to other haptophytes and rhodophytes, but not cryptophytes or stramenopiles, the mitochondrial genome has lost the nad7, nad9 and nad11 genes. The ~105 kb chloroplast genome encodes 112 protein coding genes, including ycf39 which has strong structural homology to NADP-binding nitrate transcriptional regulators; a divergent ‘CheY-like’ two-component response regulator (ycf55) and Tic/Toc (ycf60 and ycf80) membrane transporters. Notably, a zinc finger domain has been identified in the rpl36 ribosomal protein gene of all chloroplasts sequenced to date with the exception of haptophytes and cryptophytes - algae that have gained (via lateral gene transfer) an alternative rpl36 lacking the zinc finger motif. The two C. tobin chloroplast ribosomal RNA operon spacer regions differ in tRNA content. Additionally, each ribosomal operon contains multiple single nucleotide polymorphisms (SNPs) - a pattern observed in rhodophytes and cryptophytes, but few stramenopiles. Analysis of small (<200 bp) chloroplast encoded tandem and inverted repeats in C. tobin and 78 other algal chloroplast genomes show that repeat type, size and location are correlated with gene identity and taxonomic clade. CONCLUSION: The Chrysochromulina tobin organellar genomes provide new insight into organellar function and evolution. These are the first organellar genomes to be determined for the prymnesiales, a taxon that is present in both oceanic and freshwater systems and represents major primary photosynthetic producers and contributors to global ecosystem stability. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-604) contains supplementary material, which is available to authorized users. BioMed Central 2014-07-17 /pmc/articles/PMC4226036/ /pubmed/25034814 http://dx.doi.org/10.1186/1471-2164-15-604 Text en © Hovde et al.; licensee BioMed Central Ltd. 2014 This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Hovde, Blake T
Starkenburg, Shawn R
Hunsperger, Heather M
Mercer, Laina D
Deodato, Chloe R
Jha, Ramesh K
Chertkov, Olga
Monnat, Raymond J
Cattolico, Rose Ann
The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles
title The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles
title_full The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles
title_fullStr The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles
title_full_unstemmed The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles
title_short The mitochondrial and chloroplast genomes of the haptophyte Chrysochromulina tobin contain unique repeat structures and gene profiles
title_sort mitochondrial and chloroplast genomes of the haptophyte chrysochromulina tobin contain unique repeat structures and gene profiles
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4226036/
https://www.ncbi.nlm.nih.gov/pubmed/25034814
http://dx.doi.org/10.1186/1471-2164-15-604
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