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

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. ^[3]; Devarenne, Timothy P. ^[4]; Weiss, Taylor L. ^[4]; Pellegrini, Matteo ^[2]; Hackett, Jeremiah D. ^[3]

Univ. of Arizona, Tucson, AZ (United States); University of Arizona
Univ. of California Los Angeles, Los Angeles, CA (United States)
Univ. of Arizona, Tucson, AZ (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.

View Accepted Manuscript (DOE)

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

Publisher:: SpringerCopyright Statement

Country of Publication:: United States

Language:: English

References (113)

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
ChemInform Abstract: Monoterpene and Sesquiterpene Syntheses and the Origin of Terpene Skeletal Diversity in Plants. Degenhardt, Joerg; Koellner, Tobias G.; Gershenzon, Jonathan ChemInform, Vol. 41, Issue 14 https://doi.org/10.1002/chin.201014259	journal	March 2010
Autophagy: cellular and molecular mechanisms Glick, Danielle; Barth, Sandra; Macleod, Kay F. The Journal of Pathology, Vol. 221, Issue 1 https://doi.org/10.1002/path.2697	journal	February 2010
Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: With focus on proteins involved in lipid metabolism Nguyen, Hoa M.; Baudet, Mathieu; Cuiné, Stéphan PROTEOMICS, Vol. 11, Issue 21 https://doi.org/10.1002/pmic.201100114	journal	September 2011
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
Genome size and phylogenetic analysis of the A and L races of Botryococcus braunii Weiss, Taylor L.; Johnston, J. Spencer; Fujisawa, Kazuhiro Journal of Applied Phycology, Vol. 23, Issue 5 https://doi.org/10.1007/s10811-010-9586-7	journal	September 2010
Structures of some botryococcenes: branched hydrocarbons from the b-race of the green alga Botryococcus braunii Metzger, P.; Casadevall, E.; Pouet, M. J. Phytochemistry, Vol. 24, Issue 12 https://doi.org/10.1016/0031-9422(85)80043-1	journal	November 1985
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
Botryoxanthin A, a member of a new class of carotenoids from the green microalga Botryococcus braunii Berkeley Okada, Shigeru; Matsuda, Hisashi; Murakami, Masahiro Tetrahedron Letters, Vol. 37, Issue 7 https://doi.org/10.1016/0040-4039(95)02349-6	journal	February 1996
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
Xanthophylls as modulators of membrane protein function Ruban, Alexander V.; Johnson, Matthew P. Archives of Biochemistry and Biophysics, Vol. 504, Issue 1 https://doi.org/10.1016/j.abb.2010.06.034	journal	December 2010
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
On photoprotective mechanisms of carotenoids in light harvesting complex Xiao, Fu-Gui; Shen, Liang; Ji, Hong-Fang Biochemical and Biophysical Research Communications, Vol. 414, Issue 1 https://doi.org/10.1016/j.bbrc.2011.09.049	journal	October 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
Unraveling algal lipid metabolism: Recent advances in gene identification Khozin-Goldberg, Inna; Cohen, Zvi Biochimie, Vol. 93, Issue 1 https://doi.org/10.1016/j.biochi.2010.07.020	journal	January 2011
Mechanism and challenges in commercialisation of algal biofuels Singh, Anoop; Nigam, Poonam Singh; Murphy, Jerry D. Bioresource Technology, Vol. 102, Issue 1 https://doi.org/10.1016/j.biortech.2010.06.057	journal	January 2011
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
Transcriptome analysis of an oil-rich race B strain of Botryococcus braunii (BOT-70) by de novo assembly of 5′-end sequences of full-length cDNA clones Ioki, Motohide; Baba, Masato; Nakajima, Nobuyoshi Bioresource Technology, Vol. 109 https://doi.org/10.1016/j.biortech.2011.11.047	journal	April 2012
Modes of hydrocarbon oil biosynthesis revealed by comparative gene expression analysis for race A and race B strains of Botryococcus braunii Ioki, Motohide; Baba, Masato; Bidadi, Haniyeh Bioresource Technology, Vol. 109 https://doi.org/10.1016/j.biortech.2011.11.078	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
Biodiesel from algae: challenges and prospects Scott, Stuart A.; Davey, Matthew P.; Dennis, John S. Current Opinion in Biotechnology, Vol. 21, Issue 3 https://doi.org/10.1016/j.copbio.2010.03.005	journal	June 2010
Metabolic engineering of microbial pathways for advanced biofuels production Zhang, Fuzhong; Rodriguez, Sarah; Keasling, Jay D. Current Opinion in Biotechnology, Vol. 22, Issue 6 https://doi.org/10.1016/j.copbio.2011.04.024	journal	December 2011
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
New microbial fuels: a biotech perspective Rude, Mathew A.; Schirmer, Andreas Current Opinion in Microbiology, Vol. 12, Issue 3 https://doi.org/10.1016/j.mib.2009.04.004	journal	June 2009
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
Co-occurrence of long chain diols, keto-ols, hydroxy acids and keto acids in recent sediments of Lake El Junco, Galápagos Islands Zhang, Zhaohui; Metzger, Pierre; Sachs, Julian P. Organic Geochemistry, Vol. 42, Issue 7 https://doi.org/10.1016/j.orggeochem.2011.04.012	journal	August 2011
C31–C34 methylated squalenes from a Bolivian strain of Botryococcus braunii Achitouv, Etienne; Metzger, Pierre; Rager, Marie-Noëlle Phytochemistry, Vol. 65, Issue 23 https://doi.org/10.1016/j.phytochem.2004.09.015	journal	December 2004
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
The single cellular green microalga Botryococcus braunii, race B possesses three distinct 1-deoxy-d-xylulose 5-phosphate synthases Matsushima, Daisuke; Jenke-Kodama, Holger; Sato, Yohei Plant Science, Vol. 185-186 https://doi.org/10.1016/j.plantsci.2012.01.002	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
Future prospects of microalgal biofuel production systems Stephens, Evan; Ross, Ian L.; Mussgnug, Jan H. Trends in Plant Science, Vol. 15, Issue 10 https://doi.org/10.1016/j.tplants.2010.06.003	journal	October 2010
Remodeling the isoprenoid pathway in tobacco by expressing the cytoplasmic mevalonate pathway in chloroplasts Kumar, Shashi; Hahn, Frederick M.; Baidoo, Edward Metabolic Engineering, Vol. 14, Issue 1 https://doi.org/10.1016/j.ymben.2011.11.005	journal	January 2012
The biosynthetic pathway for lipoic acid is present in plastids and mitochondria in Arabidopsis thaliana¹ Yasuno, Rie; Wada, Hajime FEBS Letters, Vol. 517, Issue 1-3 https://doi.org/10.1016/s0014-5793(02)02589-9	journal	March 2002
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
Braunixanthins 1 and 2, new carotenoids from the green microalga Botryococcus braunii Okada, Shigeru; Tonegawa, Izumi; Matsuda, Hisashi Tetrahedron, Vol. 53, Issue 33 https://doi.org/10.1016/s0040-4020(97)00705-9	journal	August 1997
Biosynthesis of the triterpenoids, botryococcenes and tetramethylsqualene in the B race of Botryococcus braunii via the non-mevalonate pathway Sato, Yohei; Ito, Yusai; Okada, Shigeru Tetrahedron Letters, Vol. 44, Issue 37 https://doi.org/10.1016/s0040-4039(03)01784-2	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
Engineering microbial biofuel tolerance and export using efflux pumps Dunlop, Mary J.; Dossani, Zain Y.; Szmidt, Heather L. Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.21	journal	January 2011
Metabolic network reconstruction of Chlamydomonas offers insight into light‐driven algal metabolism Chang, Roger L.; Ghamsari, Lila; Manichaikul, Ani Molecular Systems Biology, Vol. 7, Issue 1 https://doi.org/10.1038/msb.2011.52	journal	January 2011
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
The biosynthesis of C5–C25 terpenoid compounds Dewick, Paul M. Natural Product Reports, Vol. 19, Issue 2 https://doi.org/10.1039/b002685i	journal	January 2002
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
Identification of unique mechanisms for triterpene biosynthesis in Botryococcus braunii Niehaus, T. D.; Okada, S.; Devarenne, T. P. Proceedings of the National Academy of Sciences, Vol. 108, Issue 30 https://doi.org/10.1073/pnas.1106222108	journal	July 2011
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
Raman Spectroscopy Analysis of Botryococcene Hydrocarbons from the Green Microalga Botryococcus braunii Weiss, Taylor L.; Chun, Hye Jin; Okada, Shigeru Journal of Biological Chemistry, Vol. 285, Issue 42 https://doi.org/10.1074/jbc.m110.157230	journal	August 2010
Functional Identification of Triterpene Methyltransferases from Botryococcus braunii Race B Niehaus, Tom D.; Kinison, Scott; Okada, Shigeru Journal of Biological Chemistry, Vol. 287, Issue 11 https://doi.org/10.1074/jbc.m111.316059	journal	January 2012
Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research Conesa, A.; Gotz, S.; Garcia-Gomez, J. M. Bioinformatics, Vol. 21, Issue 18 https://doi.org/10.1093/bioinformatics/bti610	journal	August 2005
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
Functional characterization of the three genes encoding 1-deoxy-D-xylulose 5-phosphate synthase in maize Cordoba, E.; Porta, H.; Arroyo, A. Journal of Experimental Botany, Vol. 62, Issue 6 https://doi.org/10.1093/jxb/erq393	journal	January 2011
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
PANTHER version 7: improved phylogenetic trees, orthologs and collaboration with the Gene Ontology Consortium Mi, Huaiyu; Dong, Qing; Muruganujan, Anushya Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp1019	journal	December 2009
The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases Caspi, Ron; Altman, Tomer; Dale, Joseph M. Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp875	journal	October 2009
KEGG for representation and analysis of molecular networks involving diseases and drugs Kanehisa, Minoru; Goto, Susumu; Furumichi, Miho Nucleic Acids Research, Vol. 38, Issue suppl_1 https://doi.org/10.1093/nar/gkp896	journal	October 2009
Reactome: a database of reactions, pathways and biological processes Croft, D.; O'Kelly, G.; Wu, G. Nucleic Acids Research, Vol. 39, Issue Database https://doi.org/10.1093/nar/gkq1018	journal	November 2010
The Pfam protein families database Punta, M.; Coggill, P. C.; Eberhardt, R. Y. Nucleic Acids Research, Vol. 40, Issue D1 https://doi.org/10.1093/nar/gkr1065	journal	November 2011
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
CAP3: A DNA Sequence Assembly Program Huang, X. Genome Research, Vol. 9, Issue 9 https://doi.org/10.1101/gr.9.9.868	journal	September 1999
Inhibition of Target of Rapamycin Signaling and Stress Activate Autophagy in Chlamydomonas reinhardtii Pérez-Pérez, María Esther; Florencio, Francisco J.; Crespo, José L. Plant Physiology, Vol. 152, Issue 4 https://doi.org/10.1104/pp.109.152520	journal	January 2010
RNA-Seq Analysis of Sulfur-Deprived Chlamydomonas Cells Reveals Aspects of Acclimation Critical for Cell Survival González-Ballester, David; Casero, David; Cokus, Shawn The Plant Cell, Vol. 22, Issue 6 https://doi.org/10.1105/tpc.109.071167	journal	June 2010
The Chlorella variabilis NC64A Genome Reveals Adaptation to Photosymbiosis, Coevolution with Viruses, and Cryptic Sex Blanc, Guillaume; Duncan, Garry; Agarkova, Irina The Plant Cell, Vol. 22, Issue 9 https://doi.org/10.1105/tpc.110.076406	journal	September 2010
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
VARIABILITY OF CELL WALL STRUCTURE AND HYDROCARBON TYPE IN DIFFERENT STRAINS OF BOTRYOCOCCUS BRAUNII ¹ Berkaloff, Claire; Rousseau, Bernard; Couté, Alain Journal of Phycology, Vol. 20, Issue 3 https://doi.org/10.1111/j.0022-3646.1984.00377.x	journal	September 1984
Chemical Profile of Selected Species of Microalgae with Emphasis on Lipids1 Ben-Amotz, Ami; Tornabene, Thomas G.; Thomas, William H. Journal of Phycology, Vol. 21, Issue 1 https://doi.org/10.1111/j.0022-3646.1985.00072.x	journal	October 2004
GROWTH AND BRANCHED HYDROCARBON PRODUCTION IN A STRAIN OF BOTRYOCOCCUS BRAUNII (CHLOROPHYTA)¹ Wolf, Fred R.; Nonomura, Arthur M.; Bassham, James A. Journal of Phycology, Vol. 21, Issue 3 https://doi.org/10.1111/j.0022-3646.1985.00388.x	journal	September 1985
Structure and Chemistry of a new Chemical race of Botryococcus Braunii (Chlorophyceae) that Produces Lycopadiene, a Tetraterpenoid Hydrocarbon1 Metzger, Pierre; Allard, Beatrice; Casadevall, Eliette Journal of Phycology, Vol. 26, Issue 2 https://doi.org/10.1111/j.0022-3646.1990.00258.x	journal	June 1990
The family of terpene synthases in plants: a mid-size family of genes for specialized metabolism that is highly diversified throughout the kingdom: Terpene synthase family Chen, Feng; Tholl, Dorothea; Bohlmann, Jörg The Plant Journal, Vol. 66, Issue 1 https://doi.org/10.1111/j.1365-313x.2011.04520.x	journal	March 2011
Phylogenetic Placement, Genome Size, and gc Content of the Liquid-Hydrocarbon-Producing Green Microalga Botryococcus Braunii Strain Berkeley (Showa) (Chlorophyta)1: b. Braunii Berkeley Genome size Weiss, Taylor L.; Spencer Johnston, J.; Fujisawa, Kazuhiro Journal of Phycology, Vol. 46, Issue 3 https://doi.org/10.1111/j.1529-8817.2010.00820.x	journal	April 2010
The Chlamydomonas Genome Reveals the Evolution of Key Animal and Plant Functions Merchant, S. S.; Prochnik, S. E.; Vallon, O. Science, Vol. 318, Issue 5848, p. 245-250 https://doi.org/10.1126/science.1143609	journal	October 2007
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
Increased Lipid Accumulation in the Chlamydomonas reinhardtii sta7-10 Starchless Isoamylase Mutant and Increased Carbohydrate Synthesis in Complemented Strains Work, Victoria H.; Radakovits, Randor; Jinkerson, Robert E. Eukaryotic Cell, Vol. 9, Issue 8 https://doi.org/10.1128/ec.00075-10	journal	June 2010
Structural Correlates of Cytoplasmic and Chloroplast Lipid Body Synthesis in Chlamydomonas reinhardtii and Stimulation of Lipid Body Production with Acetate Boost Goodson, Carrie; Roth, Robyn; Wang, Zi Teng Eukaryotic Cell, Vol. 10, Issue 12 https://doi.org/10.1128/ec.05242-11	journal	October 2011
Isoprenoid Biosynthesis in Synechocystis sp. Strain PCC6803 Is Stimulated by Compounds of the Pentose Phosphate Cycle but Not by Pyruvate or Deoxyxylulose-5-Phosphate Ershov, Y. V.; Gantt, R. R.; Cunningham, F. X. Journal of Bacteriology, Vol. 184, Issue 18 https://doi.org/10.1128/jb.184.18.5045-5051.2002	journal	September 2002
Inactivation of sll1556 in Synechocystis Strain PCC 6803 Impairs Isoprenoid Biosynthesis from Pentose Phosphate Cycle Substrates In Vitro Poliquin, K.; Ershov, Y. V.; Cunningham, F. X. Journal of Bacteriology, Vol. 186, Issue 14 https://doi.org/10.1128/jb.186.14.4685-4693.2004	journal	July 2004
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
F ROM B ACTERIAL G LYCOGEN TO S TARCH : Understanding the Biogenesis of the Plant Starch Granule Ball, Steven G.; Morell, Matthew K. Annual Review of Plant Biology, Vol. 54, Issue 1 https://doi.org/10.1146/annurev.arplant.54.031902.134927	journal	June 2003
Algal Functional Annotation Tool: a web-based analysis suite to functionally interpret large gene lists using integrated annotation and expression data Lopez, David; Casero, David; Cokus, Shawn J. BMC Bioinformatics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2105-12-282	journal	January 2011
The metagenomics RAST server – a public resource for the automatic phylogenetic and functional analysis of metagenomes Meyer, F.; Paarmann, D.; D'Souza, M. BMC Bioinformatics, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2105-9-386	journal	September 2008
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
Characterization of the Conus bullatus genome and its venom-duct transcriptome Hu, Hao; Bandyopadhyay, Pradip K.; Olivera, Baldomero M. BMC Genomics, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2164-12-60	journal	January 2011
The cellulose synthase superfamily in fully sequenced plants and algae Yin, Yanbin; Huang, Jinling; Xu, Ying BMC Plant Biology, Vol. 9, Issue 1 https://doi.org/10.1186/1471-2229-9-99	journal	January 2009
Plant Acetyl-CoA Carboxylase: Structure, Biosynthesis, Regulation, and Gene Manipulation for Plant Breeding Sasaki, Yukiko; Nagano, Yukio Bioscience, Biotechnology, and Biochemistry, Vol. 68, Issue 6 https://doi.org/10.1271/bbb.68.1175	journal	January 2004
Studies on algal carotenoids Liaaen-Jensen, S. Pure and Applied Chemistry, Vol. 61, Issue 3 https://doi.org/10.1351/pac198961030369	journal	January 1989
A Model for Carbohydrate Metabolism in the Diatom Phaeodactylum tricornutum Deduced from Comparative Whole Genome Analysis Kroth, Peter G.; Chiovitti, Anthony; Gruber, Ansgar PLoS ONE, Vol. 3, Issue 1 https://doi.org/10.1371/journal.pone.0001426	journal	January 2008
Functional Characterization of the Chlamydomonas reinhardtii ERG3 Ortholog, a Gene Involved in the Biosynthesis of Ergosterol Brumfield, Kristy M.; Moroney, James V.; Moore, Thomas S. PLoS ONE, Vol. 5, Issue 1 https://doi.org/10.1371/journal.pone.0008659	journal	January 2010
Examination of Triacylglycerol Biosynthetic Pathways via De Novo Transcriptomic and Proteomic Analyses in an Unsequenced Microalga Guarnieri, Michael T.; Nag, Ambarish; Smolinski, Sharon L. PLoS ONE, Vol. 6, Issue 10 https://doi.org/10.1371/journal.pone.0025851	journal	October 2011
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
STEROL METHYLTRANSFERASE 1 Controls the Level of Cholesterol in Plants Diener, Andrew C.; Li, Haoxia; Zhou, Wen-xu The Plant Cell, Vol. 12, Issue 6 https://doi.org/10.2307/3871215	journal	June 2000
Pigment Composition of the Green Microalga Botryococcus braunii Kawaguchi-1 Tonegawa, Izumi; Okada, Shigeru; Murakami, Masahiro Fisheries science, Vol. 64, Issue 2 https://doi.org/10.2331/fishsci.64.305	journal	January 1998
Carotenoids in Algae: Distributions, Biosyntheses and Functions Takaichi, Shinichi Marine Drugs, Vol. 9, Issue 6 https://doi.org/10.3390/md9061101	journal	June 2011
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 figshare https://doi.org/10.6084/m9.figshare.c.4845309	collection	January 2020
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 figshare https://doi.org/10.6084/m9.figshare.c.4845309.v1	collection	January 2020

Cited By (14)

Desiccation tolerance of Botryococcus braunii (Trebouxiophyceae, Chlorophyta) and extreme temperature tolerance of dehydrated cells Demura, Mikihide; Ioki, Motohide; Kawachi, Masanobu Journal of Applied Phycology, Vol. 26, Issue 1 https://doi.org/10.1007/s10811-013-0059-7	journal	July 2013
Nitrogen deprivation-induced de novo transcriptomic profiling of the oleaginous green alga Botryococcus braunii 779 Xu, Zhenyu; He, Jing; Qi, Shuyuan Genomics Data, Vol. 6 https://doi.org/10.1016/j.gdata.2015.09.019	journal	December 2015
A squalene synthase-like enzyme initiates production of tetraterpenoid hydrocarbons in Botryococcus braunii Race L Thapa, Hem R.; Naik, Mandar T.; Okada, Shigeru Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11198	journal	April 2016
De novo transcriptomic analysis of hydrogen production in the green alga Chlamydomonas moewusii through RNA-Seq Yang, Shihui; Guarnieri, Michael T.; Smolinski, Sharon Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-118	journal	January 2013
The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata Armaleo, Daniele; Müller, Olaf; Lutzoni, François BMC Genomics, Vol. 20, Issue 1 https://doi.org/10.1186/s12864-019-5629-x	journal	July 2019
Transcriptomic analysis of a moderately growing subisolate Botryococcus braunii 779 (Chlorophyta) in response to nitrogen deprivation Fang, Lei; Sun, Deying; Xu, Zhenyu Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0307-y	journal	August 2015
Comparative transcriptome analyses of oleaginous Botryococcus braunii race A reveal significant differences in gene expression upon cobalt enrichment Cheng, Pengfei; Zhou, Chengxu; Wang, Yan Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1331-5	journal	December 2018
Genetic resources for advanced biofuel production described with the Gene Ontology Torto-Alalibo, Trudy; Purwantini, Endang; Lomax, Jane Frontiers in Microbiology, Vol. 5 https://doi.org/10.3389/fmicb.2014.00528	journal	October 2014
De novo transcriptomic analysis of the oleaginous alga Botryococcus braunii AC768 (Chlorophyta) Zhang, Xiaolin; Wen, Fang; Xu, Zhenyu Journal of Applied Phycology, Vol. 31, Issue 1 https://doi.org/10.1007/s10811-018-1577-0	journal	July 2018
Algal omics: unlocking bioproduct diversity in algae cell factories Guarnieri, Michael T.; Pienkos, Philip T. Photosynthesis Research, Vol. 123, Issue 3 https://doi.org/10.1007/s11120-014-9989-4	journal	March 2014
Reconstruction of the microalga Nannochloropsis salina genome-scale metabolic model with applications to lipid production Loira, Nicolás; Mendoza, Sebastian; Paz Cortés, María BMC Systems Biology, Vol. 11, Issue 1 https://doi.org/10.1186/s12918-017-0441-1	journal	July 2017
Metabolic survey of Botryococcus braunii: Impact of the physiological state on product formation Blifernez-Klassen, Olga; Chaudhari, Swapnil; Klassen, Viktor PLOS ONE, Vol. 13, Issue 6 https://doi.org/10.1371/journal.pone.0198976	journal	June 2018
The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata Armaleo, Daniele; Müller, Olaf; Lutzoni, François BioMed Central https://doi.org/10.14288/1.0380051	text	January 2019
The lichen symbiosis re-viewed through the genomes of Cladonia grayi and its algal partner Asterochloris glomerata Daniele, Armaleo,; Olaf, Müller,; François, Lutzoni, BioMed Central https://doi.org/10.5167/uzh-175027	text	January 2019

Similar Records

Reclassification of Botryococcus braunii chemical races into separate species based on a comparative genomics analysis

Journal Article · Mon Jul 29 00:00:00 EDT 2024 · PLoS ONE · OSTI ID:2471862

A squalene synthase-like enzyme initiates production of tetraterpenoid hydrocarbons in Botryococcus braunii Race L

Journal Article · Wed Apr 06 00:00:00 EDT 2016 · Nature Communications · OSTI ID:1255082

Related Subjects

09 BIOMASS FUELS
ABC transporter
autophagy
biofuel
botryococcene
botryococcus braunii
fatty acid biosynthesis
start biosynthesis
terpene biosynthesis
transcriptome

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)*

Citation Formats

References (113)

Cited By (14)

Similar Records

Related Subjects