Botryococcus braunii: a rich source for hydrocarbons and related ether lipids

P. Metzger; C. Largeau

doi:10.1007/s00253-004-1779-z

Applied Microbiology and Biotechnology

February 2005, Volume 66, Issue 5, pp 486–496

Botryococcus braunii: a rich source for hydrocarbons and related ether lipids

Authors
Authors and affiliations

P. MetzgerEmail author
C. Largeau

Mini-Review

First Online:: 04 December 2004

Received:: 06 July 2004
Revised:: 23 September 2004
Accepted:: 24 September 2004

DOI: 10.1007/s00253-004-1779-z

Cite this article as:: Metzger, P. & Largeau, C. Appl Microbiol Biotechnol (2005) 66: 486. doi:10.1007/s00253-004-1779-z

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Abstract

This paper presents a review on Botryococcus braunii, a cosmopolitan green colonial microalga characterised by a considerable production of lipids, notably hydrocarbons. Strains like wild populations of this alga differ in the type of hydrocarbons they synthesise and accumulate: (1) n-alkadienes and trienes, (2) triterpenoid botryococcenes and methylated squalenes, or (3) a tetraterpenoid, lycopadiene. In addition to hydrocarbons and some classic lipids, these algae produce numerous series of characteristic ether lipids closely related to hydrocarbons. This review covers the algal biodiversity, the chemical structures and biosynthesis of hydrocarbons and ether lipids and the biotechnological studies related to hydrocarbon production.

References

Aaronson S, Berner T, Gold K, Kushner L, Patni NJ, Repak A, Rubin D (1983) Some observations on the green planktonic alga, Botryococcus braunii and its bloom form. J Plankton Res 5:693–700Google Scholar
Achitouv E, Metzger P, Rager M-N, Largeau C (2004) C₃₁–C₃₄ methylated squalenes from a Bolivian strain of Botryococcus braunii. Phytochemistry 65:3159–3165PubMedGoogle Scholar
An J-Y, Sim S-J, Lee JS, Kim BW (2003) Hydrocarbon production from secondarily treated piggery wastewater by the green alga Botryococcus braunii. J Appl Phycol 15:185–191CrossRefGoogle Scholar
Baillez C, Largeau C, Casadevall E (1985) Growth and hydrocarbon production of Botryococcus braunii immobilized in calcium alginate gel. Appl Microbiol Biotechnol 23:99–105CrossRefGoogle Scholar
Baillez C, Largeau C, Berkaloff C, Casadevall E (1986) Immobilization of Botryococcus braunii in alginate: influence on chlorophyll content, photosynthetic activity and degeneration during batch cultures. Appl Microbiol Biotechnol 23:361–366Google Scholar
Baillez C, Largeau C, Casadevall E, Yang LW, Berkaloff C (1988) Photosynthesis, growth and hydrocarbon production of Botryococcus braunii immobilized by entrapment and adsorption in polyurethane foams. Appl Microbiol Biotechnol 29:141–147CrossRefGoogle Scholar
Brenckmann F, Largeau C, Casadevall E, Berkaloff C (1985a) Influence de la nutrition azotée sur la croissance et la production d’hydrocarbures de l’algue Botryococcus braunii. In: Palz W, Coombs J, Hall DO (eds) Energy from biomass. Elsevier, London, pp 717–721Google Scholar
Brenckmann F, Largeau C, Casadevall E, Core C, Berkaloff C (1985b) Influence of light intensity on hydrocarbon and total biomass production of Botryococcus braunii. Relationships with photosynthetic characteristics. In: Palz W, Coombs J, Hall DO (eds) Energy from biomass. Elsevier, London, pp 722–726Google Scholar
Brown AC, Knights BA (1969) Hydrocarbon content and its relationship to physiological state in the green alga Botryococcus braunii. Phytochemistry 8:543–547CrossRefGoogle Scholar
Casadevall E, Metzger P, Puech MP (1984) Biosynthesis of triterpenoid hydrocarbons in the alga Botryococcus braunii. Tetrahedron Lett 25:4123–4126CrossRefGoogle Scholar
Casadevall E, Dif D, Largeau C, Gudin C, Chaumont D, Desanti O (1985) Studies on batch and continuous cultures of Botryococcus braunii: hydrocarbon production in relation to physiological state, cell structure, and phosphate nutrition. Biotechnol Bioeng 27:286–295Google Scholar
Cepák V, Lukavsky J (1994) The effect of high irradiances on growth, biosynthetic activities and the ultrastructure of the green alga Botryococcus braunii strain Droop 1950/807-1. Arch Hydrobiol Suppl 101:1–17Google Scholar
ChanYong T-P, Largeau C, Casadevall E (1986) Biosynthesis of non-isoprenoid hydrocarbons by the microalga Botryococcus braunii: evidence for an elongation decarboxylation mechanism; activation of decarboxylation. Nouv J Chim 10:701–707Google Scholar
Chirac C, Casadevall E, Largeau C, Metzger P (1985) Bacterial influence upon growth and hydrocarbon production of the green alga Botryococcus braunii. J Phycol 21:380–387Google Scholar
Cox RE, Burlingame AL, Wilson DM, Eglinton G, Maxwell JR (1973) Botryococcene—a tetramethylated acyclic triterpenoid of algal origin. JCS Chem Commun 12:284–285CrossRefGoogle Scholar
David M, Metzger P, Casadevall E (1988) Two cyclobotryococcenes from the B race of the green alga Botryococcus braunii. Phytochemistry 27:2863–2867CrossRefGoogle Scholar
Dennis MW, Kolattukudy PE (1991) Alkane biosynthesis by decarbonylation of aldehyde catalyzed by a microsomal preparation from Botryococcus braunii. Arch Biochem Biophys 287:268–275CrossRefPubMedGoogle Scholar
Dennis M, Kolattukudy PE (1992) A cobalt-porphirin enzyme converts a fatty aldehyde to a hydrocarbon and CO. Proc Natl Acad Sci USA 89:5306–5310PubMedGoogle Scholar
Duvold T, Cali P, Bravo JM, Rohmer M (1997) Incorporation of 2-C-methyl-d-erythritol, a putative isoprenoid precursor in the mevalonate-independent pathway, into ubiquinone and menaquinone of Escherichia coli. Tetrahedron Lett 35:6181–6184CrossRefGoogle Scholar
Frenz J, Largeau C, Casadevall E (1989a) Hydrocarbon recovery by extraction with a biocompatible solvent from free and immobilized cultures of Botryococcus braunii. Enzyme Microb Technol 11:717–724CrossRefGoogle Scholar
Frenz J, Largeau C, Casadevall E, Kollerup F, Daugulis AJ (1989b) Hydrocarbon recovery and biocompatibility of solvents for extraction from cultures of Botryococcus braunii. Biotechnol Bioeng 34:755–762Google Scholar
Galbraith MN, Hillen LW, Wake LV (1983) Darwinene: a branched hydrocarbon from a green form of Botryococcus braunii. Phytochemistry 22:1441–1443; errata (1983) Phytochemistry 22:2889CrossRefGoogle Scholar
Gudin C, Chaumont D (1981) For a solar biotechnology based on microalgae. In: Chartier P, Palz W (eds) Energy from biomass, serie E, vol 1. Reidel, Dordrecht, pp 81–84Google Scholar
Gudin C, Chaumont D (1984) Solar biotechnology study and development of tubular solar receptors for controlled production of photosynthetic cellular biomass for methane production and specific exocellular biomass. In: Palz W, Pirrwitz D (eds) Energy from biomass, serie E, vol 5. Reidel, Dordrecht, pp 184–193Google Scholar
Huang Y, Street-Perrott FA, Perrott RA, Metzger P, Eglinton G (1999) Glacial-interglacial environmental changes inferred from molecular and compound-specific δ¹³C analyses of sediments from Sacred lake, Mt. Kenya. Geochim Cosmochim 63:1383–1404CrossRefGoogle Scholar
Huang Z, Poulter CD (1988) Braunicene. Absolute stereochemistry of the cyclohexane ring. J Org Chem 53:4089–4094Google Scholar
Huang Z, Poulter CD (1989a) Tetramethylsqualene, a triterpene from Botryococcus braunii var. Showa. Phytochemistry 28:1467–1470CrossRefGoogle Scholar
Huang Z, Poulter CD (1989b) Stereochemical studies of botryococcene biosynthesis: analogies between 1′-1 and 1′-3 condensations in isoprenoid pathway. J Am Chem Soc 111:2713–2715Google Scholar
Huszar VLM, Reynolds CS (1997) Phytoplankton periodicity and sequences of dominance in an Amazonian flood-plain lake (Lago Bata, Parà, Brazil): responses to gradual environmental change. Hydrobiologia 346:169–181CrossRefGoogle Scholar
Inoue H, Korenaga T, Sagami H, Koyama T, Sugiyama H, Ogura K (1993) Formation of farnesal and 3-hydroxy-2,3-dihydrofarnesal from farnesol by protoplasts of Botryococcus braunii. Biochem Biophys Res Commun 196:1401–1405CrossRefPubMedGoogle Scholar
Inoue H, Korenaga T, Sagami H, Koyama T, Ogura K (1994a) Phosphorylation of farnesol by a cell-free system from Botryococcus braunii. Biochem Biophys Res Commun 200:1036–1041CrossRefPubMedGoogle Scholar
Inoue S, Dote Y, Sawayama S, Minowa T, Ogi T, Yokoyama S-Y (1994b) Analysis of oil derived from liquefaction of Botryococcus braunii. Biomass Bioenergy 6:269–274CrossRefGoogle Scholar
Inoue H, Sagami H, Koyama T, Ogura K (1995) Properties of farnesol phosphokinase of Botryococcus braunii. Phytochemistry 40:377–381CrossRefGoogle Scholar
Jarstfer MB, Zhang D-L, Poulter CD (2002) Recombinant squalene synthase. Synthesis of non-head-to-tail isoprenoids in the absence of NADPH. J Am Chem Soc 124:8834–8845CrossRefPubMedGoogle Scholar
Knights BA, Brown AC, Conway E, Middleditch BS (1970) Hydrocarbons from the green form of the freshwater alga Botryococcus braunii. Phytochemistry 9:1317–1324CrossRefGoogle Scholar
Kojima E, Zhang K (1999) Growth and hydrocarbons of microalga Botryococcus braunii in bubble column photobioreactors. J Biosci Bioeng 87:811–815CrossRefGoogle Scholar
Komárek J, Marvan P (1992) Morphological differences in natural populations of the genus Botryococcus (Chlorophyceae). Arch Protistendk 141:65–100Google Scholar
Largeau C, Casadevall E, Berkaloff C, Dhamelincourt P (1980) Sites of accumulation and composition of hydrocarbons in Botryococcus braunii. Phytochemistry 19:1043–1051CrossRefGoogle Scholar
Lee SJ, Kim S-B, Kwon G-S, Yoon B-B, Oh H-M (1998) Effects of harvesting method and growth stage on the flocculation of the green alga Botryococcus braunii. Lett Appl Microbiol 27:14–18CrossRefGoogle Scholar
Mangold HK, Paltauf F (1983) Ether lipids, biochemical and biomedical aspects. Academic Press, New YorkGoogle Scholar
McKirdy DM, Cox RE, Volkman JK, Howell VJ (1986) Botryococcane in a new class of Australian non-marine crude oils. Nature 320:57–59CrossRefGoogle Scholar
Mendes RL, Nobre BP, Cardoso MT, Pereira AP, Palavra AF (2003) Supercritical carbon dioxide extraction of compounds with pharmaceutical importance from microalgae. Inorg Chim Acta 356:328–334CrossRefGoogle Scholar
Metzger P (1993) n-Heptacosatrienes and tetraenes from a Bolivian strain of Botryococcus braunii. Phytochemistry 33:1125–1128CrossRefGoogle Scholar
Metzger P (1994) Phenolic ether lipids with an n-alkenylresorcinol moiety from a Bolivian strain of Botryococcus braunii (A race). Phytochemistry 36:195–212CrossRefGoogle Scholar
Metzger P (1999) Two terpenoid diepoxides from the green microalga Botryococcus braunii: their biomimetic conversion to tetrahydrofurans and tetrahydropyrans. Tetrahedron 55:167–176CrossRefGoogle Scholar
Metzger P, Casadevall E (1983) Structure de trois nouveaux botryococcènes synthétisés par une souche de Botryococcus brauniii cultivée en laboratoire. Tetrahedron Lett 24:4013–4016CrossRefGoogle Scholar
Metzger P, Casadevall E (1987) Lycopadiene, a tetraterpenoid hydrocarbon from new strains of the green alga Botryococcus braunii. Tetrahedron Lett 28:3931–3934CrossRefGoogle Scholar
Metzger P, Casadevall E (1991) Botryococcoid ethers, ether lipids from Botryococcus braunii. Phytochemistry 30:1439–1444CrossRefGoogle Scholar
Metzger P, Casadevall E (1992) Ether lipids from Botryococcus braunii and their biosynthesis. Phytochemistry 31:2341–2349CrossRefGoogle Scholar
Metzger P, Largeau C (1999) Chemicals of Botryococcus braunii. In: Cohen Z (ed) Chemicals from microalgae. Taylor & Francis, London, pp 205–260Google Scholar
Metzger P, Largeau C (2002) Natural polyacetals. In: Steinbüchel A (ed) Biopolymers, vol. 9. Wiley-VCH, Weinheim, pp 113–127Google Scholar
Metzger P, Rager M-N (2002) Lycopanerols H, two high molecular weight ether lipids from Botryococcus braunii comprising an α-tocopherol unit. Tetrahedron Lett 43:2377–2380CrossRefGoogle Scholar
Metzger P, Berkaloff C, Couté A, Casadevall E (1985a) Alkadiene- and botryococcene-producing races of wild strains of Botryococcus braunii. Phytochemistry 24:2305–2312Google Scholar
Metzger P, Casadevall E, Pouet M-J, Pouet Y (1985b) Structures of some botryococcenes: branched hydrocarbons from the B race of the green alga Botryococcus braunii. Phytochemistry 24:2995–3002CrossRefGoogle Scholar
Metzger P, Templier J, Largeau C, Casadevall E (1986) An n-alkatriene and some n-alkadienes from the A race of the green alga Botryococcus braunii. Phytochemistry 25:1869–1872CrossRefGoogle Scholar
Metzger P, David M, Casadevall E (1987) Biosynthesis of triterpenoid hydrocarbons in the B race of the green alga Botryococcus brauniii. Sites of production and nature of the methylating agent. Phytochemistry 26:129–134CrossRefGoogle Scholar
Metzger P, Allard B, Casadevall E, Berkaloff C, Couté A (1990) Structure and chemistry of a new chemical race of Botryococcus braunii that produces lycopadiene, a tetraterpenoid hydrocarbon. J Phycol 26:258–266CrossRefGoogle Scholar
Metzger P, Largeau C, Casadevall E (1991) Lipids and macromolecular lipids of the hydrocarbon-rich microalga Botryococcus braunii. Prog Chem Org Nat Prod 57:1–70Google Scholar
Metzger P, Pouet Y, Summons R (1997) Chemotaxonomic evidence for the similarity between Botryococcus braunii L race and Botryococcus neglectus. Phytochemistry 44:1071–1075CrossRefGoogle Scholar
Metzger P, Rager M-N, Largeau C (2002) Botryolins A and B, two tetramethylsqualene triethers from the green microalga Botryococcus braunii. Phytochemistry 59:839–843CrossRefPubMedGoogle Scholar
Metzger P, Rager M-N, Sellier N, Largeau C (2003) Lycopanerols I-L: four new tetraterpenoid ethers from the green microalga Botryococcus braunii. J Nat Prod 66:772–778PubMedGoogle Scholar
Moldowan JM, Seifert WK (1980) First discovery of botryococcane in petroleum. JCS Chem Commun 19:912–914CrossRefGoogle Scholar
Ohmori M, Wolf FR, Bassham JA (1984) Botryococcus braunii carbon/nitrogen metabolism as affected by ammonia addition. Arch Microbiol 140:101–106CrossRefGoogle Scholar
Okada S, Murakami M, Yamaguchi K (1995) Hydrocarbon composition of newly isolated strains of the green microalga Botryococcus braunii. J Appl Phycol 7:555–559Google Scholar
Okada S, Murakami M, Yamaguchi K (1997a) Characterization of hydrocarbons from the Yayoi strain of the green microalga Botryococcus braunii. Phytochem Anal 8:198–203CrossRefGoogle Scholar
Okada S, Tonegawa I, Matsuda H, Murakami M, Yamaguchi K (1997b) Braunixanthins 1 and 2, new carotenoids from the green micoalga Botryococcus braunii. Tetrahedron 53:11307–11316CrossRefGoogle Scholar
Okada S, Devarenne TP, Chapell J (2000) Molecular characterization of squalene synthase from the green microalga Botryococcus braunii, race B. Arch Biochem Biophys 373:307–317CrossRefPubMedGoogle Scholar
Okada S, Devarenne TP, Murakami M, Abe H, Chappell J (2004) Characterization of botryococcene synthase enzyme activity, a squalene synthase-like activity from the green microalga Botryococcus braunii, race B. Arch Biochem Biophys 422:110–118CrossRefPubMedGoogle Scholar
Pedroni P, Davison J, Beckert H, Bergman P, Benemann (2001) A proposal to establish an international network of CO₂ and greenhouse gas abatement with microalgae. J Energy Environ Res 1:136–150Google Scholar
Plain N, Largeau C, Derenne S, Couté A (1993) Variabilité morphologique de Botryococcus braunii (Chlorococcales, Chlorophyta): corrélations avec les conditions de croissance et la teneur en lipides. Phycologia 32:259–265Google Scholar
Poulter CD (1990) Biosynthesis of non-head-to-tail terpenes. Formation of 1′-1 and 1′-3 linkages. Acc Chem Res 23:70–77Google Scholar
Rager M-N, Metzger P (2000) Six novel tetraterpenoid ethers, lycopanerols B-G, and some other constituents from the green microalga Botryococcus braunii. Phytochemistry 54:427–437CrossRefPubMedGoogle Scholar
Ratledge C, Wilkinson SG (1988) An overview of microbial lipids. In: Ratledge C, Wilkinson SG (eds) Microbial lipids, vol 1. Academic Press, London pp 3–22Google Scholar
Sato T, Usui S, Nakatsuka N, Sakurai S, Tsuchiya Y, Kondo Y, Hirabayashi S (2002) Innovation of novel photobioreactor for microalgae and proposal of its usage for CO₂ fixation. (Proc 1st Congr Int Soc Appl Phycol) Int Conf Appl Algol 9:119–120
Sato Y, Ito Y, Okada S, Murakami M, Abe H (2003) Biosynthesis of the triterpenoids, botryococcenes and tetramethylsqualene in the B race of Botryococcus braunii via the non-mevalonate pathway. Tetrahedron Lett 44:7035–7037CrossRefGoogle Scholar
Sawayama S, Inoue S, Yokoyama S (1994) Continuous culture of hydrocarbon-rich microalga Botryococcus braunii in secondarily treated sewage. Appl Microbiol Biotechnol 41:729–731Google Scholar
Sawayama S, Inoue S, Dote Y, Yokoyama S-H (1995) CO₂ fixation and oil production through microalga. Energy Convers Manage 36:729–731CrossRefGoogle Scholar
Sawayama S, Minowa T, Yokoyama S-Y (1999) Possibility of renewable energy production and CO₂ mitigation by thermochemical liquefaction of microalgae. Biomass Bioenergy 17:33–39CrossRefGoogle Scholar
Schwender J, Seemann M, Lichtenthaler HK, Rohmer M (1996) 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 obliqus. Biochem J 316:73–80PubMedGoogle Scholar
Senousy HH (2003) A molecular taxonomic and morphological study of the green alga genus Botryococcus. PhD thesis, University of Newcastle, Newcastle upon Tyne
Senousy HH, Beakes GW, Hack E (2004) Phylogenetic placement of Botryococcus braunii (Trebouxiophyceae) and Botryococcus sudeticus isolate UTEX 2629 (Chlorophyceae). J Phycol 40:412–423Google Scholar
Summons RE, Metzger P, Largeau C, Murray AP, Hope JM (2002) Polymethylsqualanes from Botryococcus braunii in lacustrine sediments and cruce oils. Org Geochem 33:99–109CrossRefGoogle Scholar
Templier J, Largeau C, Casadevall E (1984) Mechanism of non-isoprenoid hydrocarbon biosynthesis in Botryococcus braunii. Phytochemistry 23:1017–1028CrossRefGoogle Scholar
Templier J, Largeau C, Casadevall E (1987) Effect of various inhibitors on biosynthesis of non-isoprenoid hydrocarbon biosynthesis in Botryococcus braunii. Phytochemistry 26:377–383CrossRefGoogle Scholar
Townsend SA (2001) Perennial domination of phytoplankton by Botryococcus and Peridinium in a discontinuously polymictic reservoir (tropical Australia). Arch Hydrobiol 151:529–548Google Scholar
Villarreal-Rosales E, Metzger P, Casadevall E (1992) Ether lipid production in relation to growth in Botryococcus braunii. Phytochemistry 31:3021–3027CrossRefGoogle Scholar
Volova TG, Kalacheva GS, Zhila NO (2003) Specificity of lipid composition in two Botryococcus strains, the producers of liquid hydrocarbons. Russ J Plant Physiol 50:627–633CrossRefGoogle Scholar
Wake LV, Hillen LW (1980) Study of a “bloom” of the oil-rich alga Botryococcus braunii in the Darwin River Reservoir. Biotechnol Bioeng 22:1637–1656Google Scholar
Wake LV, Hillen LW (1981) Nature and hydrocarbon content of blooms of the alga Botryococcus braunii occurring in Australian freshwater lakes. Aust J Mar Freshwater Res 32:353–367Google Scholar
Wang J, Yang S, Cong W, Cai Z (2003) Effect of nutrient conditions on the growth of Botryococcus braunii. Chin J Process Eng 3:141–145Google Scholar
White JD, Somers TC, Reddy GN (1986) Absolute configuration of (−) botryococcene. J Am Chem Soc 108:5352–5353Google Scholar
White JD, Somers TC, Reddy GN (1992) Degradation and absolute configurational assignment to C₃₄ botryococcene. J Org Chem 57:4991–4998Google Scholar
Wolf FR, Nemethy EK, Blanding JH, Bassham JA (1985a) Biosynthesis of unusual acyclic isoprenoids in the alga Botryococcus braunii. Phytochemistry 24:733–737CrossRefGoogle Scholar
Wolf FR, Nonomura AM, Bassham JA (1985b) Growth and branched hydrocarbon production in a strain of Botryococcus braunii (Chlorophyta). J Phycol 21:388–396Google Scholar
Yang S, Wang J, Cong W, Cai Z, Ouyang F (2004a) Utilization of nitrite as a nitrogen source by Botryococcus braunii. Biotechnol Lett 26:239–243CrossRefPubMedGoogle Scholar
Yang S, Wang J, Cong W, Cai Z, Ouyang F (2004b) Effects of bisulfite and sulfite on the microalga Botryococcus braunii. Enzyme Microb Technol 35:46–50CrossRefGoogle Scholar

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P. Metzger
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C. Largeau
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1.Laboratoire de Chimie Bioorganique et Organique PhysiqueEcole Nationale Supérieure de Chimie de ParisParisFrance

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Botryococcus braunii: a rich source for hydrocarbons and related ether lipids

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