Skip to main content
Log in

Genetic basis of microbial carotenogenesis

  • Review Article
  • Published:
International Microbiology Aims and scope Submit manuscript

Abstract.

The synthesis of carotenoids begins with the formation of a phytoene from geranylgeranyl pyrophosphate, a well conserved step in all carotenogenic organisms and catalyzed by a phytoene synthase, an enzyme encoded by the crtB (spy) genes. The next step is the dehydrogenation of the phytoene, which is carried out by phytoene dehydrogenase. In organisms with oxygenic photosynthesis, this enzyme, which accomplishes two dehydrogenations, is encoded by the crtP genes. In organisms that lack oxygenic photosynthesis, dehydrogenation is carried out by an enzyme completely unrelated to the former one, which carries out four dehydrogenations and is encoded by the crtI genes. In organisms with oxygenic photosynthesis, dehydrogenation of the phytoene is accomplished by a ζ-carotene dehydrogenase encoded by the crtQ (zds) genes. In many carotenogenic organisms, the process is completed with the cyclization of lycopene. In organisms exhibiting oxygenic photosynthesis, this step is performed by a lycopene cyclase encoded by the crtL genes. In contrast, anoxygenic photosynthetic and non-photosynthetic organisms use a different lycopene cyclase, encoded by the crtY (lyc) genes. A third and unrelated type of lycopene β-cyclase has been described in certain bacteria and archaea. Fungi differ from the rest of non-photosynthetic organisms in that they have a bifunctional enzyme that displays both phytoene synthase and lycopene cyclase activity. Carotenoids can be modified by oxygen-containing functional groups, thus originating xanthophylls. Only two enzymes are necessary for the conversion of β-carotene into astaxanthin, using several ketocarotenoids as intermediates, in both prokaryotes and eukaryotes. These enzymes are a β-carotene hydroxylase (crtZ genes) and a β-carotene ketolase, encoded by the crtW (bacteria) or bkt (algae) genes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2A, B.

Similar content being viewed by others

References

  1.  Andrews A, Phaff HJ, Starr MP (1976) Carotenoids of Phaffia rhodozyma, a red pigmented fermenting yeast. Phytochemistry 15:1003–1009

    Article  Google Scholar 

  2.  Armstrong G (1997) Genetics of eubacterial carotenoid biosynthesis: a colorful tale. Annu Rev Microbiol 51:629–659

    Article  CAS  PubMed  Google Scholar 

  3.  Arrach N, Fenández-Martín R, Cerdá-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

    CAS  PubMed  Google Scholar 

  4.  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

    CAS  PubMed  Google Scholar 

  5.  Bartley GE, Scolnik PA (1995) Plant carotenoids: pigments for photoprotection, visual attraction, and human heath. Plant Cell 7:1027–1038

    Article  CAS  PubMed  Google Scholar 

  6.  Bauer CE, Bollivar DW, Suzuki JY (1993) Genetic analyses of photopigmented biosynthesis in eubacteria: a guiding light for algae and plants. J Bacteriol 175:3919–3925

    CAS  PubMed  Google Scholar 

  7.  Briton G (1983) The biochemistry of natural pigments. Cambridge University Press, Cambridge

  8.  Chamovitz D, Misawa N, Sandmann G, Hirschberg J (1992) Molecular cloning and expression in Escherichia coli of a cyanobacterial gene coding for phytoene synthase, a carotenoid biosynthesis enzyme. FEBS Lett 296:305–310

    Article  CAS  PubMed  Google Scholar 

  9.  Cunningham FX Jr, Gantt E (1998) Genes and enzymes of carotenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 49:557–583

    CAS  Google Scholar 

  10.  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 PCC 7942. Plant Cell 6:1107–1121

    Article  CAS  PubMed  Google Scholar 

  11.  Dogbo O, Laferrière A, D'Harlingue A, Camara B (1988) Carotenoid biosynthesis: isolation and characterization of a bifunctional enzyme catalyzing the synthesis of phytoene. Proc Natl Acad Sci USA 85:7054–7058

    CAS  Google Scholar 

  12.  Fenández-González B, Sandmann G, Vioque A (1997) A new type of asymmetrically acting β-carotene ketolase is required for the synthesis of echinenone in the cyanobacterium Synechocystis sp. PCC 6803. J Biol Chem

  13.  Girard P, Falconnier B, Bricout J, Vladescu B (1994) β-Carotene producing mutants of Phaffia rhodozyma. Appl Microbiol Biotechnol 41–47

  14.  Goodwin TW (1986) Metabolism, nutrition, and function of carotenoids. Annu Rev Nutr 6:273–281

    Article  CAS  PubMed  Google Scholar 

  15.  Hable WE, Oishi KK, Schumaker KS (1998) Viviparous-5 encodes phytoene desaturase, an enzyme essential for abscisic acid (ABA) accumulation and seed development in maize. Mol Gen Genet 257:167–176

    Article  CAS  PubMed  Google Scholar 

  16.  Hausmann A, Sandman G (2000) A single five-step desaturase is involved in the carotenoid biosynthesis pathway to β-carotene and torulene in Neurospora crassa. Fungal Genet Biol 30:147–153

    Article  CAS  PubMed  Google Scholar 

  17.  Hugueney P, Badillo A, Chen H-C, Klein A, Hirschberg J, Camara B, Kuntz M (1995) Metabolism of cyclic carotenoids: a model for the alteration of this biosynthetic pathway in Capsicum annuum chromoplasts. Plant J 8:417–424

    Article  CAS  PubMed  Google Scholar 

  18.  Hundle BS, Alberti M, Nievelstein V, Beyer P, Kleinin H, Armstrong GA, Burke DH, Hearst JE (1994) Functional assignment of Erwinia herbicola Eho10 carotenoid genes expressed in Escherichia coli. Mol Gen Genet 254:406–416

    Google Scholar 

  19.  Johnson EA, An G-H (1991) Astaxanthin from microbial sources. Crit Rev Biotechnol 11:297–306

    CAS  Google Scholar 

  20.  Johnson EA, Lewis MJ (1979) Astaxanthin formation by the yeast Phaffia rhodozyma. J Gen Microbiol 115:173–183

    CAS  Google Scholar 

  21.  Johnson EA, Schroeder WA (1995) Microbial carotenoids. Adv Biochem Eng Biotechnol 53:119–178

    Google Scholar 

  22.  Kajiwara S, Kakizono T, Saito T, Kondo K, Ohtani T, Nishio N, Nagai S, Misawa N (1995) Isolation and functional identification of a novel cDNA for astaxanthin biosynthesis from Haematococcus pluvialis and astaxanthin synthesis in Escherichia coli. Plant Mol Biol 29:343–352

    CAS  PubMed  Google Scholar 

  23.  Krubasik P, Sandmann G (2000) 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

    CAS  PubMed  Google Scholar 

  24.  Linden H, Vioque A, Sandmann G (1993) Isolation of a carotenoid biosynthesis gene coding for ζ-carotene desaturase from Anabaena PCC 7120 by heterologous complementation. FEMS Microbiol Lett 106:99–104

    Article  CAS  Google Scholar 

  25.  Lotan T, Hirschberg J (1995) Cloning and expression in Escherichia coli of the gene encoding β-C-4-oxygenase that converts β-carotene to the ketocarotenoid cantaxanthin in Haematococcus pluvialis. FEBS Lett 363:125–128

    Article  Google Scholar 

  26.  Margalith PZ (1999) Production of ketocarotenoids by microalgae. Appl Microbiol Biotechnol 51:431–438

    Article  CAS  PubMed  Google Scholar 

  27.  Mayne ST (1996) Beta-carotene, carotenoids, and disease prevention in humans. FASEB J 10:690–701

    CAS  PubMed  Google Scholar 

  28.  Misawa N, Nakagawa M, Kobayashi K, Yamano S, Izawa Y, Nakamura K, Harashima K (1990) Elucidation of the Erwinia uredovora carotenoid biosynthetic pathway by functional analysis of the gene products expressed in Escherichia coli. J Bacteriol 172:6704–6712

    CAS  PubMed  Google Scholar 

  29.  Misawa N, Truesdale MR, Sandmann G, Fraser PD, Bird C, Schuch W, Bramley PM (1994) Expression of a tomato cDNA coding for phytoene synthase in Escherichia coli, phytoene formation in vivo and in vitro, and functional analysis of various truncated gene products. J Biochem 116:980–985

    CAS  PubMed  Google Scholar 

  30.  Misawa N, Satoni Y, Kondo K, Yokoyama A, Kajiwara S, Saito T, Ohtani T, Miki W (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

    CAS  PubMed  Google Scholar 

  31.  Ourisson G, Rohmer M, Poralla K (1987) Prokaryotic hopanoids and other polyterpenoid sterol surrogates. Annu Rev Microbiol 41:301–333

    Article  CAS  PubMed  Google Scholar 

  32.  Peck RF, Johnson EA, Krebs MP (2002) Identification of a lycopene β-cyclase required for bacteriorhodopsin biogenesis in the archaeon Halobacterium salinarium. J Bacteriol 184:2889–2897

    Article  CAS  PubMed  Google Scholar 

  33.  Pecker I, Chamovitz D, Linden H, Sandmann G, Hirschberg J (1992) A single polypeptide catalyzing the conversion of phytoene to ζ-carotene is transcriptionally regulated during tomato fruit ripening. Proc Natl Acad Sci USA 89:4962–4966

    CAS  PubMed  Google Scholar 

  34.  Pecker I, Gabbay R, Cunningham FX Jr, Hirschberg J (1996) Cloning and characterization of the cDNA for lycopene β-cyclase from tomato reveals decrease in its expression during fruit ripening. Plant Mol Biol 30:807–819

    CAS  PubMed  Google Scholar 

  35.  Sandmann G (1994a) Phytoene desaturase: genes, enzymes and phylogenetic aspects. J Plant Physiol 143:444–447

    CAS  Google Scholar 

  36.  Sandmann G (1994b) Carotenoid biosynthesis in microorganisms and plants. Eur J Biochem 223:7–24

    CAS  PubMed  Google Scholar 

  37.  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

    Article  CAS  PubMed  Google Scholar 

  38.  Verdoes JC, Krubasik P, Sandmann G, Ooyen AJJ van (1999) Isolation and functional characterization of a novel type of carotenoid biosynthetic gene from Xanthophyllomyces dendrorhous. Mol Gen Genet 262:453–461

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements.

The authors wish to express their deepest appreciation to the PETRI program (grant PTR1995-0572-OP), to the Xunta de Galicia (grant PR 404D 2001/4-0) and to the Ramón Areces Foundation for the financial support that made this work possible.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. G. Villa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Sieiro, C., Poza, M., de Miguel, T. et al. Genetic basis of microbial carotenogenesis. Int Microbiol 6, 11–16 (2003). https://doi.org/10.1007/s10123-003-0097-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10123-003-0097-0

Keywords

Navigation