Photosynthesis Research

, 97:141 | Cite as

Bacteriophytochromes in anoxygenic photosynthetic bacteria

  • Eric Giraud
  • André VerméglioEmail author


Since the first discovery of a bacteriophytochrome in Rhodospirillum centenum, numerous bacteriophytochromes have been identified and characterized in other anoxygenic photosynthetic bacteria. This review is focused on the biochemical and biophysical properties of bacteriophytochromes with a special emphasis on their roles in the synthesis of the photosynthetic apparatus.


Bacteriophytochrome Light-harvesting complexes Photosynthesis regulation Photosynthetic apparatus Photosynthetic bacteria 



Bacteriophytochrome photoreceptor










Photosensory core domain


Photosynthesis gene cluster


Para-hydroxy-cinnamic acid


Polyketide synthase




Photoactive yellow protein








CheY-homologuous regulator domain


  1. Alberti M, Burke DH, Hearst JE (1995) Structure and sequence of the photosynthesis gene cluster. In: Blankenship RE, Madigan MT, Bauer CE (eds) Anoxygenic photosynthetic bacteria. Kluwer, Dordrecht, pp 1083–1106Google Scholar
  2. Baca M, Borgstahl GE, Boissinot M, Burke PM, Williams DR, Slater KA, Getzoff ED (1994) Complete chemical structure of photoactive yellow protein: novel thioester-linked 4-hydroxycinnamyl chromophore and photocycle chemistry. Biochemistry 33:14369–14377PubMedCrossRefGoogle Scholar
  3. Bauer CE, Elsen S, Swem LR, Swem DL, Masuda S (2003) Redox and light regulation of gene expression in photosynthetic prokaryotes. Phil Trans R Soc Lond B Biol Sci 358:147–154CrossRefGoogle Scholar
  4. Berleman JE, Hasselbring BM, Bauer CE (2004) Hypercyst mutants in Rhodospirillum centenum identify regulatory loci involved in cyst cell differentiation. J Bacteriol 186:5834–5841PubMedCrossRefGoogle Scholar
  5. Bhoo SH, Davis SJ, Walker J, Karniol B, Vierstra RD (2001) Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414:776–779PubMedCrossRefGoogle Scholar
  6. Borucki B, von Stetten D, Seibeck S, Lamparter T, Michael N, Mroginski MA, Otto H, Murgida DH, Heyn MP, Hildebrandt P (2005) Light-induced proton release of phytochrome is coupled to the transient deprotonation of the tetrapyrrole chromophore. J Biol Chem 280:34358–34364PubMedCrossRefGoogle Scholar
  7. Braatsch S, Bernstein JR, Lessner F, Morgan J, Liao JC, Harwood CS, Beatty JT (2006) Rhodopseudomonas palustris CGA009 has two functional ppsR genes, each of which encodes a repressor of photosynthesis gene expression. Biochemistry 45:14441–14451PubMedCrossRefGoogle Scholar
  8. Braatsch S, Jeanette A, Johnson JA, Noll K, Beatty JT (2007) The O2-responsive repressor PpsR2 but not PpsR1 transduces a light signal sensed by the BphP1phytochrome in Rhodopseudomonas palustris CGA009. FEMS Microbiol Lett 272:60–64PubMedCrossRefGoogle Scholar
  9. Butler WL, Lane HC (1965) Dark transformations of phytochromes in vivo. II. Plant Physiol 40:13–17PubMedCrossRefGoogle Scholar
  10. Charbonneau H, Prusti RK, Letrong H, Sonnenburg WK, Mullaney PJ, Walsh KA, Beavo JA (1990) Identification of a noncatalytic cGMP-binding domain conserved in both the cGMP-stimulated and photoreceptor cyclic nucleotide phosphodiesterases. Proc Natl Acad Sci U S A 87:288–292PubMedCrossRefGoogle Scholar
  11. Choudhary M, Kaplan S (2000) DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2.4.1. Nucleic Acids Res 28:862–867PubMedCrossRefGoogle Scholar
  12. Cogdell RJ, Durant I, Valentine J, Lindsay JG, Schmidt K (1983) The isolation and partial characterisation of the light-harvesting pigment-protein complement of Rhodopseudomonas acidophila. Biochim Biophys Acta 722:427–435CrossRefGoogle Scholar
  13. Cogdell RJ, Gall A, Köhler J (2006) The architecture and function of the light-harvesting apparatus of purple bacteria: from single molecules to in vivo membranes. Quat Rev Biophys 39:227–324CrossRefGoogle Scholar
  14. Davis SJ, Vener AV, Vierstra RD (1999) Bacteriophytochromes: phytochrome like photoreceptors from nonphotosynthetic eubacteria. Science 286:2517–2520PubMedCrossRefGoogle Scholar
  15. Eilfeld P, Rüdiger W (1985) Absorption spectra of phytochrome intermediates. Z Naturforsch 40C:109–114Google Scholar
  16. Elsen S, Ponnampalam SN, Bauer CE (1998) CrtJ bound to distant binding sites interacts cooperatively to aerobically repress photopigment biosynthesis and light harvesting II gene expression in Rhodobacter capsulatus. J Biol Chem 273:30762–30769PubMedCrossRefGoogle Scholar
  17. Elsen S, Jaubert M, Pignol D, Giraud E (2005) PpsR: a multifaceted regulator of photosynthesis gene expression in purple bacteria. Mol Microbiol 57:17–26PubMedCrossRefGoogle Scholar
  18. Evans MB, Hawthornthwaite A, Cogdell RJ (1990) Isolation and characterisation of different B800–850 light-harvesting complexes from low-and high-light grown cells of Rhodopseudomonas palustris, strain 2.1.6. Biochim Biophys Acta 1016:71–76CrossRefGoogle Scholar
  19. Evans K, Fordham-Skelton AP, Mistry H, Reynolds CD, Lawless AM, Papiz MZ (2005) A bacteriophytochrome regulates the synthesis of LH4 complexes in Rhodopseudomonas palustris. Photosynth Res 85:169–180PubMedCrossRefGoogle Scholar
  20. Evans K, Grossmann G, Fordham-Skelton AP, Papiz MZ (2006) Small-angle X-ray scattering reveals the solution structure of a bacteriophytochrome in the catalytically active Pr state. J Mol Biol 364:655–666PubMedCrossRefGoogle Scholar
  21. Fleischman DE, Forquer I (2001) Regulation of formation of the photosynthetic system in a photosynthetic rhizobium. In: PS 2001 proceedings of the 12th international congress on photosynthesis, S4-023. CSIRO Publishing, Melbourne, AustraliaGoogle Scholar
  22. Funa N, Ozawa H, Hirata A, Horinouchi S (2006) Phenolic lipid synthesis by type III polyketide synthases is essential for cyst formation in Azotobacter vinelandii. Proc Natl Acad Sci U S A 103:6356–6361PubMedCrossRefGoogle Scholar
  23. Gardiner AT, Cogdell RJ, Takaichi S (1993) The effect of growth conditions on the light-harvesting apparatus in Rhodopseudomonas acidophila. Photosynth Res 38:159–167CrossRefGoogle Scholar
  24. Genick UK, Soltis SM, Kuhn P, Canestrelli IL, Getzoff ED (1998) Structure at 0.85 Å resolution of an early protein photocycle intermediate. Nature 392:206–209PubMedCrossRefGoogle Scholar
  25. Giraud E, Fardoux J, Fourrier N, Hannibal L, Genty B, Bouyer P, Dreyfus B, Verméglio A (2002) Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 417:202–205PubMedCrossRefGoogle Scholar
  26. Giraud E, Zappa S, Jaubert M, Hannibal L, Fardoux J, Adriano J-M, Bouyer P, Genty B, Pignol D, Verméglio A (2004) Bacteriophytochrome and regulation of the synthesis of the photosynthetic apparatus in Rhodopseudomonas palustris: pitfalls of using laboratory strains. Photochem Photobiol Sci 3:587–591PubMedCrossRefGoogle Scholar
  27. Giraud E, Zappa S, Vuillet L, Adriano J-M, Hannibal L, Fardoux J, Berthomieu C, Bouyer P, Pignol D, Verméglio A (2005a) A new type of bacteriophytochrome acts in tandem with a classical bacteriophytochrome to control the antennae synthesis in Rhodopseudomonas palustris. J Biol Chem 280:32389–32397PubMedCrossRefGoogle Scholar
  28. Giraud E, Zappa S, Vuillet L, Fardoux J, Hannibal L, Adriano J-M, Jaubert M, Bouyer P, Berthomieu C, Pignol D, Verméglio A (2005b) Characterization and function of the six bacteriophytochromes of Rhodopseudomonas palustris. In: van der Est A, Bruce D (eds) Photosynthesis: fundamental aspects to global perspectives, vol 2. Alliance Communications Group, Lawrence, Kansas, pp 535–537Google Scholar
  29. Gomelsky M, Kaplan S (1995) Genetic evidence that PpsR from Rhodobacter sphaeroides 2.4.1 functions as a repressor of puc and bchF expression. J Bacteriol 177:1634–1637PubMedGoogle Scholar
  30. Hartigan N, Tharia HA, Sweeney F, Lawless AM, Papiz MZ (2002) The 7.5-Å electron density and spectroscopic properties of a novel low-light B800 LH2 from Rhodopseudomonas palustris. Biophys J 82:963–977PubMedCrossRefGoogle Scholar
  31. Hoff WD, Dux P, Hard K, Devreese B, Nugteren-Roodzant IM, Crielaard W, Boelens R, Kaptein K, van Beeumen J, Hellingwerf KJ (1994) Thiol ester-linked p-coumaric acid as a new photoactive prosthetic group in a protein with rhodopsin-like photochemistry. Biochemistry 33:13959–13962PubMedCrossRefGoogle Scholar
  32. Hoff WD, Xie A, Van Stokkum IH, Tang XJ, Gural J, Kroon AR, Hellingwerf KJ (1999) Global conformational changes upon receptor stimulation in photoactive yellow protein. Biochemistry 38:1009–1017PubMedCrossRefGoogle Scholar
  33. Hughes J, Lamparter T, Mittmann F, Hartmann E, Gärtner W, Wilde A, Börner T (1997) A prokaryotic phytochrome. Nature 386:663PubMedCrossRefGoogle Scholar
  34. Jaubert M, Lavergne J, Fardoux J, Hannibal L, Vuillet L, Adriano JM, Bouyer P, Pignol D, Giraud E, Verméglio A (2007) A singular bacteriophytochrome acquired by lateral gene transfer. J Biol Chem 282:7320–7328PubMedCrossRefGoogle Scholar
  35. Jaubert M, Vuillet L, Hannibal L, Adriano JM, Fardoux J, Bouyer P, Bonaldi K, Fleischman D, Giraud E, Verméglio A (2008) A bacteriophytochrome regulates the synthesis of a light-harvesting complex (LH4-type) in the aerobic photosynthetic bacterium Bradyrhizobium BTAi1. J Bacteriol (in press)Google Scholar
  36. Jiang ZY, Swem LR, Rushing BG, Devanathan S, Tollin G, Bauer CE (1999) Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes. Science 285:406–409PubMedCrossRefGoogle Scholar
  37. Karniol B, Viestra RD (2003) The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties. Proc Natl Acad Sci U S A 100:2807–2812PubMedCrossRefGoogle Scholar
  38. Karniol B, Wagner JR, Walker JM, Vierstra RD (2005) Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem J 392:103–116PubMedCrossRefGoogle Scholar
  39. Kehoe DM, Grossman R (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409–1412PubMedCrossRefGoogle Scholar
  40. Kojadinovic M, Laugraud A, Vuillet L, Fardoux J, Hannibal L, Adriano J-M, Bouyer P, Giraud E, Verméglio A (2008) Dual role for a bacteriophytochrome in the bioenergetic control of Rhodopsdeudomonas palustris: enhancement of photosystem synthesis and limitation of respiration. Biochim Biophys Acta 1777:163–172PubMedCrossRefGoogle Scholar
  41. Kovacs AT, Rakhely G, Kovacs KL (2005) The PpsR regulator family. Res Microbiol 156:619–625PubMedCrossRefGoogle Scholar
  42. Kyndt JA, Meyer TE, Cusanovich MA (2004) Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria. Photochem Photobiol Sci 3:519–530PubMedCrossRefGoogle Scholar
  43. Kyndt JA, Fitch JC, Meyer TE, Cusanovich MA (2005) Thermochromatium tepidum photoactive yellow protein/bacteriophytochrome/diguanylate cyclase: characterization of the PYP domain. Biochemistry 44:4755–4764PubMedCrossRefGoogle Scholar
  44. Kyndt JA, Fitch JC, Meyer TE, Cusanovich MA (2007) The photoactivated pyp domain of Rhodospirillum centenum Ppr accelerates the recovery of the bacteriophytochrome domain after white light illumination. Biochemistry 46:8256–8262PubMedCrossRefGoogle Scholar
  45. Lamparter T, Michael N, Mittmann F, Esteban B (2002) Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an N-terminal chromophore attachment site. Proc Natl Acad Sci U S A 99:11628–11633PubMedCrossRefGoogle Scholar
  46. Larimer FW, Chain P, Hauser L, Lamerdin J, Malfatti S, Do L, Land ML, Pelletier DA, Beatty JT, Lang AS et al (2004) Complete genome sequence of the metabolically versatile photosynthetic bacterium Rhodopseudomonas palustris. Nat Biotechnol 22:55–61PubMedCrossRefGoogle Scholar
  47. Masuda S, Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613–623PubMedCrossRefGoogle Scholar
  48. Masuda S, Dong C, Swem D, Setterdahl AT, Knaff DB, Bauer CE (2002) Repression of photosynthesis gene expression by formation of a disulfide bond in CrtJ. Proc Natl Acad Sci U S A 99:7078–7083PubMedCrossRefGoogle Scholar
  49. Meyer TE (1985) Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophilic phototrophic bacterium Ectothiorhodospira halophila. Biochim Biophy Acta 806:175–183CrossRefGoogle Scholar
  50. Moskvin OV, Gomelsky L, Gomelsky M (2005) Transcriptome analysis of the Rhodobacter sphaeroides PpsR regulon: PpsR as a master regulator of photosystem development. J Bacteriol 187:2148–2156PubMedCrossRefGoogle Scholar
  51. Oh JI, Kaplan S (2000) Redox signalling: globalisation of gene expression. EMBO J 19:4237–4247PubMedCrossRefGoogle Scholar
  52. Oh JI, Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39:1116–1123PubMedCrossRefGoogle Scholar
  53. Ponnampalam SN, Bauer CE (1997) DNA binding characteristics of CrtJ. A redox-responding repressor of bacteriochlorophyll, carotenoid, and light harvesting-II gene expression in Rhodobacter capsulatus. J Biol Chem 272:18391–18396PubMedCrossRefGoogle Scholar
  54. Purcell EB, Crosson S (2008) Photoregulation in prokaryotes. Curr Opin Microbiol 11:168–178PubMedCrossRefGoogle Scholar
  55. Quail PH, Boylan MT, Parks BM, Short TW, Xu Y, Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268:675–680PubMedCrossRefGoogle Scholar
  56. Ragatz L, Jiang ZY, Bauer CE, Gest H (1994) Phototactic purple bacteria. Nature 370:104CrossRefGoogle Scholar
  57. Rockwell NC, Su YS, Lagarias JC (2006) Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57:837–858PubMedCrossRefGoogle Scholar
  58. Smith H (2000) Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407:585–591PubMedCrossRefGoogle Scholar
  59. Tadros MH, Waterkamp K (1989) Multiple copies of the coding regions for the light-harvesting B800–850 alpha- and beta-polypeptides are present in the Rhodopseudomonas palustris genome. EMBO J 8:1303–1308PubMedGoogle Scholar
  60. Tarutina M, Ryjenkov DA, Gomelsky M (2006) An unorthodox bacteriophytochrome from Rhodobacter sphaeroides involved in turnover of the second messenger c-di-GMP. J Biol Chem 281:34751–34758PubMedCrossRefGoogle Scholar
  61. van Brederode ME, Hoff WD, Van Stockkum IHM, Groot ML, Hellingwerf KJ (1996) Protein folding thermodynamics applied to the photocycle of the photoactive yellow protein. Biophys J 71:365–380PubMedGoogle Scholar
  62. Vuillet L, Kojadinovic M, Zappa S, Jaubert M, Adriano JM, Fardoux J, Hannibal L, Pignol D, Verméglio A, Giraud E (2007) Evolution of a bacteriophytochrome from light to redox sensor. EMBO J 6:3322–3331CrossRefGoogle Scholar
  63. Wagner JR, Brunzelle JS, Forest KT, Vierstra RD (2005) A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 438:325–331PubMedCrossRefGoogle Scholar
  64. Yang X, Stojkovic EA, Kuk J, Moffat K (2007) Crystal structure of the chromophore binding domain of an unusual bacteriophytochrome, RpBphP3, reveals residues that modulate photoconversion. Proc Natl Acad Sci U S A 104:12571–12576PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  1. 1.Laboratoire des Symbioses Tropicales et MéditerranéennesIRD, CIRAD, AGRO-M, INRA, UM2Montpellier Cedex 5France
  2. 2.CEA, DSV, IBEB, Lab Bioenerget CellulaireSaint-Paul-lez-DuranceFrance
  3. 3.CNRS, UMR Biol Veget & Microbiol EnvironSaint-Paul-lez-DuranceFrance
  4. 4.Aix-Marseille UniversitéSaint-Paul-lez-DuranceFrance

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