Bio-crude transcriptomics: Gene discovery and metabolic network reconstruction for the biosynthesis of the terpenome of the hydrocarbon oil-producing green alga, Botryococcus braunii race B (Showa)*

Molnár, István; Lopez, David; Wisecaver, Jennifer H.; Devarenne, Timothy P.; Weiss, Taylor L.; Pellegrini, Matteo; Hackett, Jeremiah D.

doi:10.1186/1471-2164-13-576

Title: Bio-crude transcriptomics: Gene discovery and metabolic network reconstruction for the biosynthesis of the terpenome of the hydrocarbon oil-producing green alga, Botryococcus braunii race B (Showa)*

Journal Article · Tue Oct 30 00:00:00 EDT 2012 · BMC Genomics

DOI:https://doi.org/10.1186/1471-2164-13-576· OSTI ID:1093677

Molnár, István ^[1]; Lopez, David ^[2]; Wisecaver, Jennifer H. ^[1]; Devarenne, Timothy P. ^[3]; Weiss, Taylor L. ^[3]; Pellegrini, Matteo ^[2]; Hackett, Jeremiah D. ^[1]

Univ. of Arizona, Tucson, AZ (United States)
Univ. of California Los Angeles, Los Angeles, CA (United States)
Texas A & M Univ., College Station, TX (United States)

Microalgae hold promise for yielding a biofuel feedstock that is sustainable, carbon-neutral, distributed, and only minimally disruptive for the production of food and feed by traditional agriculture. Amongst oleaginous eukaryotic algae, the B race of Botryococcus braunii is unique in that it produces large amounts of liquid hydrocarbons of terpenoid origin. These are comparable to fossil crude oil, and are sequestered outside the cells in a communal extracellular polymeric matrix material. The biosynthetic engineering of terpenoid bio-crude production requires identification of genes and reconstruction of metabolic pathways responsible for production of both hydrocarbons and other metabolites of the alga that compete for photosynthetic carbon and energy.

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Research Organization:: Univ. of Arizona, Tucson, AZ (United States)

Sponsoring Organization:: USDOE Office of Energy Efficiency and Renewable Energy (EERE)

Grant/Contract Number:: EE0003046

OSTI ID:: 1093677

Journal Information:: BMC Genomics, Vol. 13, Issue 1; ISSN 1471-2164

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 36 works

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References (49)

Phylloquinone, what can we learn from plants? Lochner, K.; Döring, O.; Böttger, M. BioFactors, Vol. 18, Issue 1-4 https://doi.org/10.1002/biof.5520180209	journal	January 2003
Molecular Characterization of Squalene Synthase from the Green Microalga Botryococcus braunii, Race B Okada, Shigeru; Devarenne, Timothy P.; Chappell, Joseph Archives of Biochemistry and Biophysics, Vol. 373, Issue 2 https://doi.org/10.1006/abbi.1999.1568	journal	January 2000
Triacylglycerol profiling of microalgae strains for biofuel feedstock by liquid chromatography–high-resolution mass spectrometry MacDougall, Karen M.; McNichol, Jesse; McGinn, Patrick J. Analytical and Bioanalytical Chemistry, Vol. 401, Issue 8 https://doi.org/10.1007/s00216-011-5376-6	journal	September 2011
Botryococcus braunii: a rich source for hydrocarbons and related ether lipids Metzger, P.; Largeau, C. Applied Microbiology and Biotechnology, Vol. 66, Issue 5 https://doi.org/10.1007/s00253-004-1779-z	journal	December 2004
Biosynthesis and engineering of isoprenoid small molecules Withers, Sydnor T.; Keasling, Jay D. Applied Microbiology and Biotechnology, Vol. 73, Issue 5 https://doi.org/10.1007/s00253-006-0593-1	journal	November 2006
Botryococcene distribution in strains of the green alga Botryococcus braunii Metzger, P.; Casadevall, E.; Coute, A. Phytochemistry, Vol. 27, Issue 5 https://doi.org/10.1016/0031-9422(88)80199-7	journal	January 1988
Glycerolipid Biosynthesis Riekhof, Wayne R.; Benning, Christoph The Chlamydomonas Sourcebook, Vol. 2, 41-68 https://doi.org/10.1016/b978-0-12-370873-1.00010-1	book	January 2009
Characterization of botryococcene synthase enzyme activity, a squalene synthase-like activity from the green microalga Botryococcus braunii, Race B Okada, Shigeru; Devarenne, Timothy P.; Murakami, Masahiro Archives of Biochemistry and Biophysics, Vol. 422, Issue 1 https://doi.org/10.1016/j.abb.2003.12.004	journal	February 2004
Enzymes of the mevalonate pathway of isoprenoid biosynthesis Miziorko, Henry M. Archives of Biochemistry and Biophysics, Vol. 505, Issue 2 https://doi.org/10.1016/j.abb.2010.09.028	journal	January 2011
Apoptosis, autophagy, and more Lockshin, Richard A.; Zakeri, Zahra The International Journal of Biochemistry & Cell Biology, Vol. 36, Issue 12 https://doi.org/10.1016/j.biocel.2004.04.011	journal	December 2004
The versatility of algae and their lipid metabolism Harwood, John L.; Guschina, Irina A. Biochimie, Vol. 91, Issue 6 https://doi.org/10.1016/j.biochi.2008.11.004	journal	June 2009
Transcriptome analysis of an oil-rich race B strain of Botryococcus braunii (BOT-22) by de novo assembly of pyrosequencing cDNA reads Ioki, Motohide; Baba, Masato; Nakajima, Nobuyoshi Bioresource Technology, Vol. 109 https://doi.org/10.1016/j.biortech.2011.08.104	journal	April 2012
Biodiesel from microalgae Chisti, Yusuf Biotechnology Advances, Vol. 25, Issue 3, p. 294-306 https://doi.org/10.1016/j.biotechadv.2007.02.001	journal	May 2007
Aquatic phototrophs: efficient alternatives to land-based crops for biofuels Dismukes, G. Charles; Carrieri, Damian; Bennette, Nicholas Current Opinion in Biotechnology, Vol. 19, Issue 3 https://doi.org/10.1016/j.copbio.2008.05.007	journal	June 2008
Hormone Signalling Crosstalk in Plant Growth Regulation Depuydt, Stephen; Hardtke, Christian S. Current Biology, Vol. 21, Issue 9 https://doi.org/10.1016/j.cub.2011.03.013	journal	May 2011
Polyacetals based on polymethylsqualene diols, precursors of algaenan in Botryococcus braunii race B Metzger, Pierre; Rager, Marie-Noëlle; Largeau, Claude Organic Geochemistry, Vol. 38, Issue 4 https://doi.org/10.1016/j.orggeochem.2006.12.003	journal	April 2007
Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants Degenhardt, Jörg; Köllner, Tobias G.; Gershenzon, Jonathan Phytochemistry, Vol. 70, Issue 15-16 https://doi.org/10.1016/j.phytochem.2009.07.030	journal	October 2009
Isoprenoid biosynthesis in eukaryotic phototrophs: A spotlight on algae Lohr, Martin; Schwender, Jörg; Polle, Jürgen E. W. Plant Science, Vol. 185-186 https://doi.org/10.1016/j.plantsci.2011.07.018	journal	April 2012
Lipids and lipid metabolism in eukaryotic algae Guschina, Irina A.; Harwood, John L. Progress in Lipid Research, Vol. 45, Issue 2 https://doi.org/10.1016/j.plipres.2006.01.001	journal	March 2006
Engineering microbial cell factories for biosynthesis of isoprenoid molecules: beyond lycopene Klein-Marcuschamer, Daniel; Ajikumar, Parayil Kumaran; Stephanopoulos, Gregory Trends in Biotechnology, Vol. 25, Issue 9 https://doi.org/10.1016/j.tibtech.2007.07.006	journal	September 2007
Biodiesel from microalgae beats bioethanol Chisti, Yusuf Trends in Biotechnology, Vol. 26, Issue 3 https://doi.org/10.1016/j.tibtech.2007.12.002	journal	March 2008
Plant ABC proteins – a unified nomenclature and updated inventory Verrier, Paul J.; Bird, David; Burla, Bo Trends in Plant Science, Vol. 13, Issue 4 https://doi.org/10.1016/j.tplants.2008.02.001	journal	April 2008
Hydrocarbon content and its relationship to physiological state in the green alga Botryococcus braunii Brown, A. C.; Knights, B. A.; Conway, Elsie Phytochemistry, Vol. 8, Issue 3 https://doi.org/10.1016/s0031-9422(00)85397-2	journal	March 1969
Aldehydes, very long chain alkenylphenols, epoxides and other lipids from an alkadiene-producing strain of Botryococcus braunii Metzger, P.; Casadevall, E. Phytochemistry, Vol. 28, Issue 8 https://doi.org/10.1016/s0031-9422(00)97927-5	journal	January 1989
Enzyme mechanisms for sterol C -methylations Nes, W. David Phytochemistry, Vol. 64, Issue 1 https://doi.org/10.1016/s0031-9422(03)00349-2	journal	September 2003
Recombinant Squalene Synthase. A Mechanism for the Rearrangement of Presqualene Diphosphate to Squalene Blagg, Brian S. J.; Jarstfer, Michael B.; Rogers, Daniel H. Journal of the American Chemical Society, Vol. 124, Issue 30 https://doi.org/10.1021/ja020411a	journal	July 2002
Characterization of Microalgal Carotenoids by Mass Spectrometry and Their Bioavailability and Antioxidant Properties Elucidated in Rat Model Ranga Rao, A.; Raghunath Reddy, R. L.; Baskaran, V. Journal of Agricultural and Food Chemistry, Vol. 58, Issue 15 https://doi.org/10.1021/jf101187k	journal	July 2010
The biosynthesis of C5–C25 terpenoid compounds Dewick, Paul M. Natural Product Reports, Vol. 16, Issue 1 https://doi.org/10.1039/a708935j	journal	January 1999
Biosynthesis of isoprenoids (carotenoids, sterols, prenyl side-chains of chlorophylls and plastoquinone) via a novel pyruvate/glyceraldehyde 3-phosphate non-mevalonate pathway in the green alga Scenedesmus obliquus Schwender, Jörg; Seemann, Myriam; Lichtenthaler, Hartmut K. Biochemical Journal, Vol. 316, Issue 1 https://doi.org/10.1042/bj3160073	journal	May 1996
Two families of sterol methyltransferases are involved in the first and the second methylation steps of plant sterol biosynthesis Bouvier-Nave, Pierrette; Husselstein, Tania; Benveniste, Pierre European Journal of Biochemistry, Vol. 256, Issue 1 https://doi.org/10.1046/j.1432-1327.1998.2560088.x	journal	August 1998
Studies on the nonmevalonate terpene biosynthetic pathway: Metabolic role of IspH (LytB) protein Rohdich, F.; Hecht, S.; Gartner, K. Proceedings of the National Academy of Sciences, Vol. 99, Issue 3 https://doi.org/10.1073/pnas.032658999	journal	January 2002
An unusual isopentenyl diphosphate isomerase found in the mevalonate pathway gene cluster from Streptomyces sp. strain CL190 Kaneda, Kazuhide; Kuzuyama, Tomohisa; Takagi, Motoki Proceedings of the National Academy of Sciences, Vol. 98, Issue 3 https://doi.org/10.1073/pnas.98.3.932	journal	January 2001
CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes Parra, G.; Bradnam, K.; Korf, I. Bioinformatics, Vol. 23, Issue 9 https://doi.org/10.1093/bioinformatics/btm071	journal	March 2007
An overview of the wcd EST clustering tool Hazelhurst, Scott; Hide, Winston; Lipták, Zsuzsanna Bioinformatics, Vol. 24, Issue 13 https://doi.org/10.1093/bioinformatics/btn203	journal	May 2008
TagDust--a program to eliminate artifacts from next generation sequencing data Lassmann, T.; Hayashizaki, Y.; Daub, C. O. Bioinformatics, Vol. 25, Issue 21 https://doi.org/10.1093/bioinformatics/btp527	journal	September 2009
Tocochromanol functions in plants: antioxidation and beyond Falk, Jon; Munné-Bosch, Sergi Journal of Experimental Botany, Vol. 61, Issue 6 https://doi.org/10.1093/jxb/erq030	journal	April 2010
KAAS: an automatic genome annotation and pathway reconstruction server Moriya, Y.; Itoh, M.; Okuda, S. Nucleic Acids Research, Vol. 35, Issue S2, p. W182-W185 https://doi.org/10.1093/nar/gkm321	journal	May 2007
Using the miraEST Assembler for Reliable and Automated mRNA Transcript Assembly and SNP Detection in Sequenced ESTs Chevreux, Bastien; Pfisterer, Thomas; Drescher, Bernd Genome Research, Vol. 14, Issue 6, p. 1147-1159 https://doi.org/10.1101/gr.1917404	journal	May 2004
Systems Biology Approach in Chlamydomonas Reveals Connections between Copper Nutrition and Multiple Metabolic Steps Castruita, Madeli; Casero, David; Karpowicz, Steven J. The Plant Cell, Vol. 23, Issue 4 https://doi.org/10.1105/tpc.111.084400	journal	April 2011
Genomic Analysis of Organismal Complexity in the Multicellular Green Alga Volvox carteri Prochnik, S. E.; Umen, J.; Nedelcu, A. M. Science, Vol. 329, Issue 5988 https://doi.org/10.1126/science.1188800	journal	July 2010
Phytohormones in algae Tarakhovskaya, E. R.; Maslov, Yu. I.; Shishova, M. F. Russian Journal of Plant Physiology, Vol. 54, Issue 2 https://doi.org/10.1134/s1021443707020021	journal	April 2007
Evolution and Diversity of Plant Cell Walls: From Algae to Flowering Plants Popper, Zoë A.; Michel, Gurvan; Hervé, Cécile Annual Review of Plant Biology, Vol. 62, Issue 1 https://doi.org/10.1146/annurev-arplant-042110-103809	journal	June 2011
Biosynthesis of Plant Isoprenoids: Perspectives for Microbial Engineering Kirby, James; Keasling, Jay D. Annual Review of Plant Biology, Vol. 60, Issue 1 https://doi.org/10.1146/annurev.arplant.043008.091955	journal	June 2009
Transcriptome analysis reveals nuclear-encoded proteins for the maintenance of temporary plastids in the dinoflagellate Dinophysis acuminata Wisecaver, Jennifer H.; Hackett, Jeremiah D. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-366	journal	January 2010
Comparing de novo assemblers for 454 transcriptome data Kumar, Sujai; Blaxter, Mark L. BMC Genomics, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2164-11-571	journal	January 2010
Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: Pathway description and gene discovery for production of next-generation biofuels Rismani-Yazdi, Hamid; Haznedaroglu, Berat Z.; Bibby, Kyle BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-148	journal	March 2011
Studies on algal carotenoids Liaaen-Jensen, S. Pure and Applied Chemistry, Vol. 61, Issue 3 https://doi.org/10.1351/pac198961030369	journal	January 1989
The Gene Ontology in 2010: extensions and refinements. Consortium, Gene Ontology Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52153	text	January 2010
Carotenoids in Algae: Distributions, Biosyntheses and Functions Takaichi, Shinichi Marine Drugs, Vol. 9, Issue 6 https://doi.org/10.3390/md9061101	journal	June 2011

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Title: Bio-crude transcriptomics: Gene discovery and metabolic network reconstruction for the biosynthesis of the terpenome of the hydrocarbon oil-producing green alga, Botryococcus braunii race B (Showa)*

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