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Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype

BACKGROUND: Improvement in the performance of eukaryotic microalgae for biofuel and bioproduct production is largely dependent on characterization of metabolic mechanisms within the cell. The marine diatom Cyclotella cryptica, which was originally identified in the Aquatic Species Program, is a prom...

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Autores principales: Traller, Jesse C., Cokus, Shawn J., Lopez, David A., Gaidarenko, Olga, Smith, Sarah R., McCrow, John P., Gallaher, Sean D., Podell, Sheila, Thompson, Michael, Cook, Orna, Morselli, Marco, Jaroszewicz, Artur, Allen, Eric E., Allen, Andrew E., Merchant, Sabeeha S., Pellegrini, Matteo, Hildebrand, Mark
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5124317/
https://www.ncbi.nlm.nih.gov/pubmed/27933100
http://dx.doi.org/10.1186/s13068-016-0670-3
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author Traller, Jesse C.
Cokus, Shawn J.
Lopez, David A.
Gaidarenko, Olga
Smith, Sarah R.
McCrow, John P.
Gallaher, Sean D.
Podell, Sheila
Thompson, Michael
Cook, Orna
Morselli, Marco
Jaroszewicz, Artur
Allen, Eric E.
Allen, Andrew E.
Merchant, Sabeeha S.
Pellegrini, Matteo
Hildebrand, Mark
author_facet Traller, Jesse C.
Cokus, Shawn J.
Lopez, David A.
Gaidarenko, Olga
Smith, Sarah R.
McCrow, John P.
Gallaher, Sean D.
Podell, Sheila
Thompson, Michael
Cook, Orna
Morselli, Marco
Jaroszewicz, Artur
Allen, Eric E.
Allen, Andrew E.
Merchant, Sabeeha S.
Pellegrini, Matteo
Hildebrand, Mark
author_sort Traller, Jesse C.
collection PubMed
description BACKGROUND: Improvement in the performance of eukaryotic microalgae for biofuel and bioproduct production is largely dependent on characterization of metabolic mechanisms within the cell. The marine diatom Cyclotella cryptica, which was originally identified in the Aquatic Species Program, is a promising strain of microalgae for large-scale production of biofuel and bioproducts, such as omega-3 fatty acids. RESULTS: We sequenced the nuclear genome and methylome of this oleaginous diatom to identify the genetic traits that enable substantial accumulation of triacylglycerol. The genome is comprised of highly methylated repetitive sequence, which does not significantly change under silicon starved lipid induction, and data further suggests the primary role of DNA methylation is to suppress DNA transposition. Annotation of pivotal glycolytic, lipid metabolism, and carbohydrate degradation processes reveal an expanded enzyme repertoire in C. cryptica that would allow for an increased metabolic capacity toward triacylglycerol production. Identification of previously unidentified genes, including those involved in carbon transport and chitin metabolism, provide potential targets for genetic manipulation of carbon flux to further increase its lipid phenotype. New genetic tools were developed, bringing this organism on a par with other microalgae in terms of genetic manipulation and characterization approaches. CONCLUSIONS: Functional annotation and detailed cross-species comparison of key carbon rich processes in C. cryptica highlights the importance of enzymatic subcellular compartmentation for regulation of carbon flux, which is often overlooked in photosynthetic microeukaryotes. The availability of the genome sequence, as well as advanced genetic manipulation tools enable further development of this organism for deployment in large-scale production systems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0670-3) contains supplementary material, which is available to authorized users.
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spelling pubmed-51243172016-12-08 Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype Traller, Jesse C. Cokus, Shawn J. Lopez, David A. Gaidarenko, Olga Smith, Sarah R. McCrow, John P. Gallaher, Sean D. Podell, Sheila Thompson, Michael Cook, Orna Morselli, Marco Jaroszewicz, Artur Allen, Eric E. Allen, Andrew E. Merchant, Sabeeha S. Pellegrini, Matteo Hildebrand, Mark Biotechnol Biofuels Research BACKGROUND: Improvement in the performance of eukaryotic microalgae for biofuel and bioproduct production is largely dependent on characterization of metabolic mechanisms within the cell. The marine diatom Cyclotella cryptica, which was originally identified in the Aquatic Species Program, is a promising strain of microalgae for large-scale production of biofuel and bioproducts, such as omega-3 fatty acids. RESULTS: We sequenced the nuclear genome and methylome of this oleaginous diatom to identify the genetic traits that enable substantial accumulation of triacylglycerol. The genome is comprised of highly methylated repetitive sequence, which does not significantly change under silicon starved lipid induction, and data further suggests the primary role of DNA methylation is to suppress DNA transposition. Annotation of pivotal glycolytic, lipid metabolism, and carbohydrate degradation processes reveal an expanded enzyme repertoire in C. cryptica that would allow for an increased metabolic capacity toward triacylglycerol production. Identification of previously unidentified genes, including those involved in carbon transport and chitin metabolism, provide potential targets for genetic manipulation of carbon flux to further increase its lipid phenotype. New genetic tools were developed, bringing this organism on a par with other microalgae in terms of genetic manipulation and characterization approaches. CONCLUSIONS: Functional annotation and detailed cross-species comparison of key carbon rich processes in C. cryptica highlights the importance of enzymatic subcellular compartmentation for regulation of carbon flux, which is often overlooked in photosynthetic microeukaryotes. The availability of the genome sequence, as well as advanced genetic manipulation tools enable further development of this organism for deployment in large-scale production systems. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s13068-016-0670-3) contains supplementary material, which is available to authorized users. BioMed Central 2016-11-25 /pmc/articles/PMC5124317/ /pubmed/27933100 http://dx.doi.org/10.1186/s13068-016-0670-3 Text en © The Author(s) 2016 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. 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
Traller, Jesse C.
Cokus, Shawn J.
Lopez, David A.
Gaidarenko, Olga
Smith, Sarah R.
McCrow, John P.
Gallaher, Sean D.
Podell, Sheila
Thompson, Michael
Cook, Orna
Morselli, Marco
Jaroszewicz, Artur
Allen, Eric E.
Allen, Andrew E.
Merchant, Sabeeha S.
Pellegrini, Matteo
Hildebrand, Mark
Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
title Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
title_full Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
title_fullStr Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
title_full_unstemmed Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
title_short Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
title_sort genome and methylome of the oleaginous diatom cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5124317/
https://www.ncbi.nlm.nih.gov/pubmed/27933100
http://dx.doi.org/10.1186/s13068-016-0670-3
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