Abstract
A carotenoid synthesis gene cluster was isolated from a marine bacterium Algoriphagus sp. strain KK10202C that synthesized flexixanthin. Seven genes were transcribed in the same direction, among which five of them were involved in carotenoid synthesis. This cluster had a unique gene organization, with an isoprenoid gene, ispH (previously named lytB), being present among the carotenoid synthesis genes. The lycopene β-cyclase encoded by the crtY cd gene appeared to be a fusion of bacterial heterodimeric lycopene cyclase CrtYc and CrtYd. This was the first time that a fusion-type of lycopene β-cyclase was reported in eubacteria. Heterologous expression of the Algoriphagus crtY cd gene in lycopene-accumulating Escherichia coli produced bicyclic β-carotene. A biosynthesis pathway for monocyclic flexixanthin was proposed in Algoriphagus sp. strain KK10202C, though several of the carotenoid synthesis genes not linked with the cluster have not yet been cloned.
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References
Aasen AJ, Jensen SL (1966) Bacterial carotenoids: the structures of flexixanthin and deoxy-flexixanthin. Acta Chem Scand 20:1970–1988
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Arrach N, Fernandez-Martin R, Cerda-Olmedo E, Avalos J (2001) A single gene for lycopene cyclase, phytoene synthase, and regulation of carotene biosynthesis in Phycomyces. Proc Natl Acad Sci USA 98:1687–1692
Arrach N, Schmidhauser TJ, Avalos J (2002) Mutants of the carotene cyclase domain of al-2 from Neurospora crassa. Mol Genet Genomics 266:914–921
Britton G, Liaaen-Jensen S, Pfander H (eds) (2004) Carotenoids handbook. Birkhauser Verlag, Basel
Cole JR et al (2005) The ribosomal database project (RDP-II): sequences and tools for high-throughput rRNA analysis. Nucleic Acids Res 1:D294–D296
Cunningham FX Jr, Lafond TP, Gantt E (2000) Evidence of a role for LytB in the nonmevalonate pathway of isoprenoid biosynthesis. J Bacteriol 182:5841–5848
Cunningham FX Jr, Pogson B, Sun Z, McDonald KA, DellaPenna D, Gantt E (1996) Functional analysis of the beta and epsilon lycopene cyclase enzymes of Arabidopsis reveals a mechanism for control of cyclic carotenoid formation. Plant Cell 8:1613–1626
Cunningham FX Jr, Sun Z, Chamovitz D, Hirschberg J, Gantt E (1994) Molecular structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp strain PCC7942. Plant Cell 6:1107–1121
Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791
Futterer O et al (2004) Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci USA 101:9091–9096
Garrity GM, Holt JG (2001) Taxonomic outline of the archaea and bacteria. In: Boone DR, Castenholz RW (eds) Bergey’s manual of systematic bacteriology. Springer, Berlin Heidelberg New York, pp 155–166
Giraud E et al (2004) Two distinct crt gene clusters for two different functional classes of carotenoid in Bradyrhizobium. J Biol Chem 279:15076–15083
Hahn FM, Hurlburt AP, Poulter CD (1999) Escherichia coli open reading frame 696 is idi, a nonessential gene encoding isopentenyl diphosphate isomerase. J Bacteriol 181:4499–4504
Hannibal L et al (2000) Isolation and characterization of canthaxanthin biosynthesis genes from the photosynthetic bacterium Bradyrhizobium sp. strain ORS278. J Bacteriol 182:3850–3853
Hemmi H, Ikejiri S, Nakayama T, Nishino T (2003) Fusion-type lycopene beta-cyclase from a thermoacidophilic archaeon Sulfolobus solfataricus. Biochem Biophys Res Commun 305:586–591
Hugueney P et al (1995) Metabolism of cyclic carotenoids: a model for the alteration of this biosynthetic pathway in Capsicum annuum chromoplasts. Plant J 8:417–424
Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Krubasik P, Sandmann G (2000a) A carotenogenic gene cluster from Brevibacterium linens with novel lycopene cyclase genes involved in the synthesis of aromatic carotenoids. Mol Gen Genet 263:423–432
Krubasik P, Sandmann G (2000b) Molecular evolution of lycopene cyclases involved in the formation of carotenoids with ionone end groups. Biochem Soc Trans 28:806–810
Krugel H, Krubasik P, Weber K, Saluz HP, Sandmann G (1999) Functional analysis of genes from Streptomyces griseus involved in the synthesis of isorenieratene, a carotenoid with aromatic end groups, revealed a novel type of carotenoid desaturase. Biochim Biophys Acta 1439:57–64
Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163
Matsuo Y, Suzuki M, Kasai H, Shizuri Y, Harayama S (2003) Isolation and phylogenetic characterization of bacteria capable of inducing differentiation in the green alga Monostroma oxyspermum. Environ Microbiol 5:25–35
McAteer S, Coulson A, McLennan N, Masters M (2001) The lytB gene of Escherichia coli is essential and specifies a product needed for isoprenoid biosynthesis. J Bacteriol 183:7403–7407
Misawa N et al (1995) Structure and functional analysis of a marine bacterial carotenoid biosynthesis gene cluster and astaxanthin biosynthetic pathway proposed at the gene level. J Bacteriol 177:6575–6584
Nedashkovskaya OI et al (2004) Description of Algoriphagus aquimarinus sp. nov., Algoriphagus chordae sp. nov. and Algoriphagus winogradskyi sp. nov., from sea water and algae, transfer of Hongiella halophila Yi and Chun 2004 to the genus Algoriphagus as Algoriphagus halophilus comb. nov. and emended descriptions of the genera Algoriphagus Bowman et al. 2003 and Hongiella Yi and Chun 2004. Int J Syst Evol Microbiol 54:1757–1764
Pasamontes L, Hug D, Tessier M, Hohmann HP, Schierle J, van Loon AP (1997) Isolation and characterization of the carotenoid biosynthesis genes of Flavobacterium sp. strain R1534. Gene 185:35–41
Peck RF, Johnson EA, Krebs MP (2002) Identification of a lycopene beta-cyclase required for bacteriorhodopsin biogenesis in the archaeon Halobacterium salinarum. J Bacteriol 184:2889–2897
Pecker I, Gabbay R, Cunningham FX Jr, Hirschberg J (1996) Cloning and characterization of the cDNA for lycopene beta-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol Biol 30:807–819
Rohdich F et al (2002) Studies on the nonmevalonate terpene biosynthetic pathway: metabolic role of IspH (LytB) protein. Proc Natl Acad Sci USA 99:1158–1163
Rohmer M, Seemann M, Horbach S, Bringer-Meyer S, Sarm H (1996) Glyceraldehyde-3-phosphate and pyruvate as precursors of isoprenic units in an alternative non-mevalonate pathway for terpenoid biosynthesis. J Am Chem Soc 118:2564–2566
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425
Schnurr G, Misawa N, Sandmann G (1996) Expression, purification and properties of lycopene cyclase from Erwinia uredovora. Biochem J 315(Pt 3):869–874
Tao L, Picataggio S, Rouviere PE, Cheng Q (2004) Asymmetrically acting lycopene β-cyclases (CrtLm) from non-photosynthetic bacteria. Mol Gen Genomics 271:180–188
Teramoto M, Takaichi S, Inomata Y, Ikenaga H, Misawa N (2003) Structural and functional analysis of a lycopene beta-monocyclase gene isolated from a unique marine bacterium that produces myxol. FEBS Lett 545:120–126
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
Velayos A, Eslava AP, Iturriaga EA (2000) A bifunctional enzyme with lycopene cyclase and phytoene synthase activities is encoded by the carRP gene of Mucor circinelloides. Eur J Biochem 267:5509–5519
Verdoes JC, Krubasik KP, Sandmann G, van Ooyen AJ (1999) Isolation and functional characterisation of a novel type of carotenoid biosynthetic gene from Xanthophyllomyces dendrorhous. Mol Gen Genet 262:453–461
Viveiros M, Krubasik P, Sandmann G, Houssaini-Iraqui M (2000) Structural and functional analysis of the gene cluster encoding carotenoid biosynthesis in Mycobacterium aurum A+. FEMS Microbiol Lett 187:95–101
Wilding EI et al (2000) Identification, evolution, and essentiality of the mevalonate pathway for isopentenyl diphosphate biosynthesis in gram-positive cocci. J Bacteriol 182:4319–4327
Yokoyama A, Miki W (1995) Composition and presumed biosynthetic pathway of carotenoids in the astaxanthin-producing bacterium Agrobacterium aurantiacum. FEMS Microbiol Lett 128:139–144
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We thank DuPont Macromolecule Analysis Lab for DNA sequencing.
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Tao, L., Yao, H., Kasai, H. et al. A carotenoid synthesis gene cluster from Algoriphagus sp. KK10202C with a novel fusion-type lycopene β-cyclase gene. Mol Genet Genomics 276, 79–86 (2006). https://doi.org/10.1007/s00438-006-0121-0
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DOI: https://doi.org/10.1007/s00438-006-0121-0