Abstract
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.
Similar content being viewed by others
Abbreviations
- BphP:
-
Bacteriophytochrome photoreceptor
- BV:
-
Biliverdin
- H :
-
Halorhodospira
- LH:
-
Light-harvesting
- PCB:
-
Phycocyanobilin
- PCD:
-
Photosensory core domain
- PGC:
-
Photosynthesis gene cluster
- pHCA:
-
Para-hydroxy-cinnamic acid
- PKS:
-
Polyketide synthase
- PS:
-
Photosystem
- PYP:
-
Photoactive yellow protein
- Rb :
-
Rhodobacter
- Rps :
-
Rhodopseudomonas
- Rs :
-
Rhodospirillum
- REC:
-
CheY-homologuous regulator domain
References
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 1083–1106
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 33:14369–14377
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 358:147–154
Berleman JE, Hasselbring BM, Bauer CE (2004) Hypercyst mutants in Rhodospirillum centenum identify regulatory loci involved in cyst cell differentiation. J Bacteriol 186:5834–5841
Bhoo SH, Davis SJ, Walker J, Karniol B, Vierstra RD (2001) Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414:776–779
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 280:34358–34364
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 45:14441–14451
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 272:60–64
Butler WL, Lane HC (1965) Dark transformations of phytochromes in vivo. II. Plant Physiol 40:13–17
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 87:288–292
Choudhary M, Kaplan S (2000) DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2.4.1. Nucleic Acids Res 28:862–867
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 722:427–435
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 39:227–324
Davis SJ, Vener AV, Vierstra RD (1999) Bacteriophytochromes: phytochrome like photoreceptors from nonphotosynthetic eubacteria. Science 286:2517–2520
Eilfeld P, Rüdiger W (1985) Absorption spectra of phytochrome intermediates. Z Naturforsch 40C:109–114
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 273:30762–30769
Elsen S, Jaubert M, Pignol D, Giraud E (2005) PpsR: a multifaceted regulator of photosynthesis gene expression in purple bacteria. Mol Microbiol 57:17–26
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 1016:71–76
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 85:169–180
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 364:655–666
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, Australia
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 103:6356–6361
Gardiner AT, Cogdell RJ, Takaichi S (1993) The effect of growth conditions on the light-harvesting apparatus in Rhodopseudomonas acidophila. Photosynth Res 38:159–167
Genick UK, Soltis SM, Kuhn P, Canestrelli IL, Getzoff ED (1998) Structure at 0.85 Å resolution of an early protein photocycle intermediate. Nature 392:206–209
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 417:202–205
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 3:587–591
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 280:32389–32397
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 535–537
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 177:1634–1637
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 82:963–977
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 33:13959–13962
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 38:1009–1017
Hughes J, Lamparter T, Mittmann F, Hartmann E, Gärtner W, Wilde A, Börner T (1997) A prokaryotic phytochrome. Nature 386:663
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 282:7320–7328
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)
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 285:406–409
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 100:2807–2812
Karniol B, Wagner JR, Walker JM, Vierstra RD (2005) Phylogenetic analysis of the phytochrome superfamily reveals distinct microbial subfamilies of photoreceptors. Biochem J 392:103–116
Kehoe DM, Grossman R (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409–1412
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 1777:163–172
Kovacs AT, Rakhely G, Kovacs KL (2005) The PpsR regulator family. Res Microbiol 156:619–625
Kyndt JA, Meyer TE, Cusanovich MA (2004) Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria. Photochem Photobiol Sci 3:519–530
Kyndt JA, Fitch JC, Meyer TE, Cusanovich MA (2005) Thermochromatium tepidum photoactive yellow protein/bacteriophytochrome/diguanylate cyclase: characterization of the PYP domain. Biochemistry 44:4755–4764
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 46:8256–8262
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 99:11628–11633
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 22:55–61
Masuda S, Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613–623
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 99:7078–7083
Meyer TE (1985) Isolation and characterization of soluble cytochromes, ferredoxins and other chromophoric proteins from the halophilic phototrophic bacterium Ectothiorhodospira halophila. Biochim Biophy Acta 806:175–183
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 187:2148–2156
Oh JI, Kaplan S (2000) Redox signalling: globalisation of gene expression. EMBO J 19:4237–4247
Oh JI, Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39:1116–1123
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 272:18391–18396
Purcell EB, Crosson S (2008) Photoregulation in prokaryotes. Curr Opin Microbiol 11:168–178
Quail PH, Boylan MT, Parks BM, Short TW, Xu Y, Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268:675–680
Ragatz L, Jiang ZY, Bauer CE, Gest H (1994) Phototactic purple bacteria. Nature 370:104
Rockwell NC, Su YS, Lagarias JC (2006) Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57:837–858
Smith H (2000) Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407:585–591
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 8:1303–1308
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 281:34751–34758
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 71:365–380
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 6:3322–3331
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 438:325–331
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 104:12571–12576
Author information
Authors and Affiliations
Corresponding author
Additional information
An erratum to this article can be found at http://dx.doi.org/10.1007/s11120-008-9362-6
Rights and permissions
About this article
Cite this article
Giraud, E., Verméglio, A. Bacteriophytochromes in anoxygenic photosynthetic bacteria. Photosynth Res 97, 141–153 (2008). https://doi.org/10.1007/s11120-008-9323-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-008-9323-0