Tetrapyrroles pp 208-220 | Cite as

Synthesis and Role of Bilins in Photosynthetic Organisms

  • Nicole Frankenberg-Dinkel
  • Matthew J. Terry
Part of the Molecular Biology Intelligence Unit book series (MBIU)


Bilins are linear tetrapyrroles that function as the chromophores of the light-harvesting phycobiliproteins and light-signalling phytochromes in photosynthetic organisms. The biosynthesis of bilins proceeds through a ferredoxin-dependent heme oxygenase that oxidises heme to biliverdin IXα, the precursor of all functional bilins in these organisms. Biliverdin IXα is subsequently converted to one of three major bilin classes, phytochromobilin, phycocyanobilin and phycoerythrobilin, by a recently discovered family of related ferredoxin-dependent bilin reductases. Bilins are usually bound to apo-proteins through single or double covalent linkages and can be further modified during this process. This reaction is autocatalytic for the photoreceptor phytochrome but requires special lyases for phycobiliproteins. The binding to the latter results in a great diversity of bilin chromophores that completely span the visible light spectrum.


Heme Oxygenase Photosynthetic Organism COOH COOH Ferredoxin Oxidoreductase Visible Light Spectrum 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Montgomery BL, Lagarias JC. Phytochrome ancestry: Sensors of bilins and light. Trends Plant Sci 2002; 7:357–366.CrossRefPubMedGoogle Scholar
  2. 2.
    Grossman AR, Bhaya D, Apt KE, Kehoe DM. Light-harvesting complexes in oxygenic photosynthesis: Diversity, control, and evolution. Annu Rev Genet 1995; 29:231–288.CrossRefPubMedGoogle Scholar
  3. 3.
    Beale SI. Biosynthesis of phycobilins. Chem Rev 1993; 93:785–802.CrossRefGoogle Scholar
  4. 4.
    Terry MJ. Analysis of bilins. In: Smith AG, Witty M, eds. Heme, Chlorophyll and Bilins. Totowa: Humana Press, 2002:273–291.Google Scholar
  5. 5.
    Sidler W. Phycobilisomes and phycobiliprotein structure. In: Bryant DA, ed. The Molecular Biology of Cyanobacteria. Dordrecht: Kluwer Academic Publishers, 1994:139–216.Google Scholar
  6. 6.
    Litts JC, Kelly JM, Lagarias JC. Structurefunction studies on phytochrome. Preliminary characterization of highly purified phytochrome from Avena sativa enriched in the 124-kilodalton species. J Biol Chem 1983; 258:11025–11031.PubMedGoogle Scholar
  7. 7.
    Yeh KC, Wu SH, Murphy JT et al. A cyanobacterial phytochrome two-component light sensory system. Science 1997; 277:1505–1508.CrossRefPubMedGoogle Scholar
  8. 8.
    Hübschmann T, Börner T, Hartmann E et al. Characterization of the Cphl holo-phytochrome from Synchocystis sp. PCC 6803. Eur J Biochem 2001; 268:2055–2063.CrossRefPubMedGoogle Scholar
  9. 9.
    Ratliff M, Zhu W, Deshmukh R et al. Homologues of Neisserial heme oxygenase in gram-negative bacteria: Degradation of heme by the product of the pigA gene of Pseudomonas aeruginosa. J Bacteriol 2001; 183:6394–6403.CrossRefPubMedGoogle Scholar
  10. 10.
    Ortiz de Montellano PR, Wilks A. Adv Inorg Chem 2000; 51:359–407.CrossRefGoogle Scholar
  11. ll.
    Muramoto T, Tsurui N, Terry MJ et al. Expression and biochemical properties of a ferredoxin-dependent heme oxygenase required for phytochrome chromophore synthesis. Plant Physiol 2002; 130:1958–1966.CrossRefPubMedGoogle Scholar
  12. 12.
    Cornejo J, Beale SI. Algal heme oxygenase from Cyanidium caldarium. Partial purification and fractionation into three required protein components. J Biol Chem 1988; 263:11915–11921.PubMedGoogle Scholar
  13. 13.
    Cornejo J, Beale SI. Phycobilin biosynthetic reactions in extracts of cyanobacteria. Photosynth Res 1997; 51:223–230.CrossRefGoogle Scholar
  14. 14.
    Frankenberg N, Lagarias JC. Phycocyanobilin: Ferredoxin oxidoreductase of Anabaena sp. PCC 7120. Biochemical and spectroscopic characterization. J Biol Chem 2003; 278:9219–9226.CrossRefPubMedGoogle Scholar
  15. 15.
    Rhie GE, Beale SI. Phycobilin biosynthesis: Reductant requirements and product identification for heme oxygenase from Cyanidium caldarium. Arch Bioch Biophys 1995; 320:182–194.CrossRefGoogle Scholar
  16. 16.
    Cornejo J, Willows RD, Beale SI. Phytobilin biosynthesis: Cloning and expression of a gene encoding soluble ferredoxin-dependent heme oxygenase from Synechocystis sp. PCC 6803. Plant J 1998; 15:99–107.CrossRefPubMedGoogle Scholar
  17. 17.
    Kaneko T, Sato S, Kotani H et al. Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 1996; 3:109–136.CrossRefPubMedGoogle Scholar
  18. 18.
    Richaud C, Zabulon G. The heme oxygenase gene (pbsA) in the red alga Rhodella violacea is discontinuous and transcriptionally activated during iron limitation. Proc Natl Acad Sci USA 1997; 94:11736–11741.CrossRefPubMedGoogle Scholar
  19. 19.
    Koornneef M, Rolff E, Spruit CJP. Genetic Control of light-inhibited hypocotyl elongation in Arabidopsis thaliana L. Heynh. Z Pflanzenphys 1980; 100:147–160.Google Scholar
  20. 20.
    Muramoto T, Kohchi T, Yokota A et al. The Arabidopsis photomorphogenic mutant hy1 is deficient in phytochrome chromophore biosynthesis as a result of a mutation in a plastid heme oxygenase. Plant Cell 1999; 11:335–347.CrossRefPubMedGoogle Scholar
  21. 21.
    Davis SJ, Kurepa J, Vierstra R. The Arabidopsis thaliana HY1 locus, required for phytochrome-chromophore biosynthesis, encodes a protein related to heme oxygenases. Proc Natl Acad Sci USA 1999; 96:6541–6546.CrossRefPubMedGoogle Scholar
  22. 22.
    Davis SJ, Bhoo SH, Durski AM et al. The heme-oxygenase family required for phytochrome chromophore biosynthesis is necessary for proper photomorphogenesis in higher plants. Plant Physiol 2001; 126:656–669.CrossRefPubMedGoogle Scholar
  23. 23.
    Terry MJ, Linley PJ, Kohchi T. Making light of it: The role of plant haem oxygenases in phytochrome chromophore synthesis. Biochem Soc Trans 2002; 30:604–609.CrossRefPubMedGoogle Scholar
  24. 24.
    Kohchi T, Mukougawa K, Frankenberg N et al. The Arabidopsis HY2 gene encodes phytochromobilin synthase, a ferredoxin-dependent biliverdin reductase. Plant Cell 2001; 13:425–436.CrossRefPubMedGoogle Scholar
  25. 25.
    Frankenberg N, Mukougawa K, Kohchi T et al. Functional genomic analysis of the HY2 family of ferredoxin-dependent bilin reductases from oxygenic photosynthetic organisms. Plant Cell 2001; 13:965–978.CrossRefPubMedGoogle Scholar
  26. 26.
    Frankenberg N, Lagarias JC. Biosynthesis and biological functions of bilins. In: Kadish KM, Smith KM, Guilard R, eds. The Porphyrin Handbook. Vol 13. New York: Elsevier Science, 2003:211–234.Google Scholar
  27. 27.
    McDowell MT, Lagarias JC. Purification and properties of phytochromobilin synthase from etiolated oat seedlings. Plant Physiol 2001; 126:1546–1554.CrossRefPubMedGoogle Scholar
  28. 28.
    Wu SH, Lagarias JC. The methylotrophic yeast Pichia pastoris synthesizes a functionally active chromophore precursor of the plant photoreceptor phytochrome. Proc Natl Acad Sci USA 1996; 93:8989–8994.CrossRefPubMedGoogle Scholar
  29. 29.
    Beale SI, Cornejo J. Enzymic transformation of biliverdin to phycocyanobilin by extracts of the unicellular red alga Cyanidium caldarium. Plant Physiol 1984; 76:7–15.CrossRefPubMedGoogle Scholar
  30. 30.
    Beale SI, Cornejo J. Biosynthesis of phycobilins. Ferredoxin-mediated reduction of biliverdin catalyzed by extracts of Cyanidium caldarium. J Biol Chem 1991; 266:22328–22332.PubMedGoogle Scholar
  31. 31.
    Beale SI, Cornejo J. Biosynthesis of phycobilins. 3(Z)-Phycoerythrobilin and 3(Z)-phycocyanobilin are intermediates in the formation of 3(E)-phycocyanobilin from biliverdin IXα. J Biol Chem 1991; 266:22333–22340.PubMedGoogle Scholar
  32. 32.
    Beale SI, Cornejo J. Biosynthesis of phycobilins. 15,16-Dihydrobiliverdin IXα is a partially reduced intermediate in the formation of phycobilins from biliverdin IXα. J Biol Chem 1991; 266:22341–22345.PubMedGoogle Scholar
  33. 33.
    Wilbanks SM, Glazer AN. Rod structure of a phycoerythrin-II-containing phycobilisome 1. Organization and sequence of the gene cluster encoding the major phycobiliprotein rod components in the genome of marine Synechococcus sp.WH8020. J Biol Chem 1993; 268:1226–1235.PubMedGoogle Scholar
  34. 34.
    Kami C, Mukougawa K, Muramoto T et al. Complementation of phytochrome chromophoredeficient Arabidopsis by expression of phycocyanobilin: Ferredoxin oxidoreductase. Proc Natl Acad Sci USA 2004; 101:1099–1104.CrossRefPubMedGoogle Scholar
  35. 35.
    Tu SL, Gunn A, Toney MD et al. Biliverdin reduction by cyanobacterial phycocyanobilin:ferredoxin oxidoreductase (PcyA) proceeds via linear tetrapyrrole radical intermediates. J Am Chem Soc 2004; 126:8682–8693.CrossRefPubMedGoogle Scholar
  36. 36.
    Wu SH, McDowell MT, Lagarias JC. Phycocyanobilin is the natural precursor of the phytochrome chromophore in the green alga Mesotaenium caldariorum. J Biol Chem 1997; 272:25700–25705.CrossRefPubMedGoogle Scholar
  37. 37.
    Wüthrich KL, Bovet L, Hunziker PE et al. Molecular cloning, functional expression and characterization of RCC reductase involved in chlorophyll catabolism. Plant J 2000; 21:189–198.CrossRefPubMedGoogle Scholar
  38. 38.
    Matile P, Hörtensteiner S. Chlorophyll degradation. Annu Rev Plant Physiol 1999; 50:67–95.CrossRefGoogle Scholar
  39. 39.
    Schluchter WM, Glazer AN. Characterization of cyanobacterial biliverdin reductase—Conversion of biliverdin to bilirubin is important for normal phycobiliprotein biosynthesis. J Biol Chem 1997; 272:13562–13569.CrossRefPubMedGoogle Scholar
  40. 40.
    Lagarias JC, Lagarias DM. Self assembly of synthetic phytochrome holoprotein in vitro. Proc Natl Acad Sci USA 1989; 86:5778–5780.CrossRefPubMedGoogle Scholar
  41. 41.
    Wu SH, Lagarias JC. Defining the bilin lyase domain: Lessons from the extended phytochrome superfamily. Biochemistry 2000; 39:13487–13495.CrossRefPubMedGoogle Scholar
  42. 42.
    Montgomery BL, Yeh KC, Crepeau MW et al. Modification of distinct aspects of photomorphogenesis via targeted expression of mammalian biliverdin reductase in transgenic Arabidopsis plants. Plant Physiol 1999; 121:629–639.CrossRefPubMedGoogle Scholar
  43. 43.
    Arciero DM, Bryant DA, Glazer AN. In vitro attachment of bilins to apophycocyanin. I. Specific covalent adduct formation at cysteinyl residues involved in phycocyanobilin binding in C-phycocyanin. J Biol Chem 1988; 263:18343–18349.PubMedGoogle Scholar
  44. 44.
    Arciero DM, Dallas JL, Glazer AN. In vitro attachment of bilins to allophycocyanin. II. Determination of the structures of tryptic bilin peptides derived from the phycocyanobilin adduct. J Biol Chem 1988; 263:18350–18357.PubMedGoogle Scholar
  45. 45.
    Arciero DM, Dallas JL, Glazer AN. In vitro attachment of bilins to allophycocyanin. III. Properties of the phycoerythrobilin adduct. J Biol Chem 1988; 263:18358–18363.PubMedGoogle Scholar
  46. 46.
    Fairchild CD, Zhao JD, Zhou JH et al. Phycocyanin alpha-subunit phycocyanobilin lyase. Proc Natl Acad Sci USA 1992; 89:7017–7021.CrossRefPubMedGoogle Scholar
  47. 47.
    Tooley AJ, Cai YA, Glazer AN. Biosynthesis of a fluorescent cyanobacterial C-phycocyanin holo-α subunit in a heterologous host. Proc Natl Acad Sci USA 2001; 98:10560–10565.CrossRefPubMedGoogle Scholar
  48. 48.
    Zhao KH, Deng MG, Zheng M et al. Novel activity of a phycobiliprotein lyase: Both the attachment of phycocyanobilin and the isomerization to phycoviolobilin are catalyzed by the proteins PecE and PecF encoded by the phycoerythrocyanin operon. FEBS Lett 2000; 469:9–13.CrossRefPubMedGoogle Scholar
  49. 49.
    Storf M, Parbel A, Meyer M et al. Chromophore attachment to biliproteins: Specificity of PecE/ PecF, a lyase-isomerase for the photoactive 31-Cys-α84-phycoviolobilin chromophore of phycoerythrocyanin. Biochemistry 2001; 40:12444–12456.CrossRefPubMedGoogle Scholar
  50. 50.
    Zhao KH, Wu D, Wang L et al. Characterization of phycoviolobilin phycoerythrocyanin-alpha 84-cystein-lyase-(isomerizing) from Mastigocladus laminosus. Eur J Biochem 2002; 269:4542–4550.CrossRefPubMedGoogle Scholar
  51. 51.
    Bhoo SH, Davis SJ, Walker J et al. Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 2001; 414:776–779.CrossRefPubMedGoogle Scholar
  52. 52.
    Lamparter T, Michael N, Mittmann F et al. Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an N-terminal chromophore attachment site. Proc Natl Acad Sci USA 2002; 99:11628–11633.CrossRefPubMedGoogle Scholar
  53. 53.
    Grossman AR, Bhaya D, He Q. Tracking the light environment by cyanobacteria and the dynamic nature of light harvesting. J Biol Chem 2001; 276:11449–11452.CrossRefPubMedGoogle Scholar
  54. 54.
    Kehoe DM, Grossman AR. Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 1996; 273:1409–1412.CrossRefPubMedGoogle Scholar
  55. 55.
    Falchuk KH, Contin JM, Dziedzic TS et al. A role for biliverdin IXα in dorsal axis development of Xenopus laevis embryos. Proc Natl Acad Sci USA 2002; 99:251–256.CrossRefPubMedGoogle Scholar
  56. 56.
    Cornah JE, Terry MJ, Smith AG. Green or red: What stops the traffic in the tetrapyrrole pathway? Trends Plant Sci 2003; 8:224–230.CrossRefPubMedGoogle Scholar
  57. 57.
    Moss GP. Nomenclature of tetrapyrroles. Recommendations 1986 IUPAC-IUB Joint Commission on Biochemical Nomenclature (JCBN). Eur J Biochem 1988; 178:277–328.CrossRefPubMedGoogle Scholar
  58. 58.
    Dammeyer T, Frankenberg-Dinkel N. Insights into phycoerythrobilin biosynthesis point toward metabolic channeling. J Biol Chem 2006; 281:27081–27089.CrossRefPubMedGoogle Scholar
  59. 59.
    Dammeyer T, Bagby SC, Sullivan MB et al. Efficient phage-mediated pigment biosynthesis in oceanic cyanobacteria. Curr Biol 2008; 18:442–448.CrossRefPubMedGoogle Scholar
  60. 60.
    Dammeyer T, Hofmann E, Frankenberg-Dinkel N. Phycoerythrobilin synthase (PebS) of a marine virus: Crystal structure of the biliverdin-complex and the substrate free form. J Biol Chem 2008; 283:27547–27554.CrossRefPubMedGoogle Scholar
  61. 61.
    Hagiwara Y, Sugishima M, Takahashi Y, Fukuyama K. Crystal structure of phycocyanobilin:ferredoxin oxidoreductase in complex with biliverdin IXalpha, a key enzyme in the biosynthesis of phycocyanobilin. Proc Natl Acad Sci USA 2006; 103:27–32.CrossRefPubMedGoogle Scholar
  62. 62.
    Tu SL, Rockwell NC, Lagarias JC, Fisher AJ. Insight into the radical mechanism of phycocyanobilin-ferredoxin oxidoreductase (PcyA) revealed by X-ray crystallography and biochemical measurements. Biochemistry 2007; 46:1484–1494.CrossRefPubMedGoogle Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  1. 1.Physiology of MicroorganismsRuhr-University BochumBochumGermany
  2. 2.School of Biological SciencesUniversity of SouthamptonSouthamptonUK

Personalised recommendations