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Bacteriophytochromes in anoxygenic photosynthetic bacteria

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An Erratum to this article was published on 10 September 2008

An Erratum to this article was published on 10 September 2008

An Erratum to this article was published on 10 September 2008

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.

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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

    Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Bhoo SH, Davis SJ, Walker J, Karniol B, Vierstra RD (2001) Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 414:776–779

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Butler WL, Lane HC (1965) Dark transformations of phytochromes in vivo. II. Plant Physiol 40:13–17

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Choudhary M, Kaplan S (2000) DNA sequence analysis of the photosynthesis region of Rhodobacter sphaeroides 2.4.1. Nucleic Acids Res 28:862–867

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Davis SJ, Vener AV, Vierstra RD (1999) Bacteriophytochromes: phytochrome like photoreceptors from nonphotosynthetic eubacteria. Science 286:2517–2520

    Article  PubMed  CAS  Google Scholar 

  • Eilfeld P, Rüdiger W (1985) Absorption spectra of phytochrome intermediates. Z Naturforsch 40C:109–114

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Hughes J, Lamparter T, Mittmann F, Hartmann E, Gärtner W, Wilde A, Börner T (1997) A prokaryotic phytochrome. Nature 386:663

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kehoe DM, Grossman R (1996) Similarity of a chromatic adaptation sensor to phytochrome and ethylene receptors. Science 273:1409–1412

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Kovacs AT, Rakhely G, Kovacs KL (2005) The PpsR regulator family. Res Microbiol 156:619–625

    Article  PubMed  CAS  Google Scholar 

  • Kyndt JA, Meyer TE, Cusanovich MA (2004) Photoactive yellow protein, bacteriophytochrome, and sensory rhodopsin in purple phototrophic bacteria. Photochem Photobiol Sci 3:519–530

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Masuda S, Bauer CE (2002) AppA is a blue light photoreceptor that antirepresses photosynthesis gene expression in Rhodobacter sphaeroides. Cell 110:613–623

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Oh JI, Kaplan S (2000) Redox signalling: globalisation of gene expression. EMBO J 19:4237–4247

    Article  PubMed  CAS  Google Scholar 

  • Oh JI, Kaplan S (2001) Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39:1116–1123

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Purcell EB, Crosson S (2008) Photoregulation in prokaryotes. Curr Opin Microbiol 11:168–178

    Article  PubMed  CAS  Google Scholar 

  • Quail PH, Boylan MT, Parks BM, Short TW, Xu Y, Wagner D (1995) Phytochromes: photosensory perception and signal transduction. Science 268:675–680

    Article  PubMed  CAS  Google Scholar 

  • Ragatz L, Jiang ZY, Bauer CE, Gest H (1994) Phototactic purple bacteria. Nature 370:104

    Article  Google Scholar 

  • Rockwell NC, Su YS, Lagarias JC (2006) Phytochrome structure and signaling mechanisms. Annu Rev Plant Biol 57:837–858

    Article  PubMed  CAS  Google Scholar 

  • Smith H (2000) Phytochromes and light signal perception by plants—an emerging synthesis. Nature 407:585–591

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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Correspondence to André Verméglio.

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An erratum to this article can be found at http://dx.doi.org/10.1007/s11120-008-9362-6

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Giraud, E., Verméglio, A. Bacteriophytochromes in anoxygenic photosynthetic bacteria. Photosynth Res 97, 141–153 (2008). https://doi.org/10.1007/s11120-008-9323-0

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