The dark recovery rate in the photocycle of the bacterial photoreceptor YtvA is affected by the cellular environment and by hydration

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Pennacchietti, Francesca ^a   Abbruzzetti, Stefania ^b,c   Losi, Aba ^b   Mandalari, Carmen ^b   Bedotti, Roberta ^b   Viappiani, Cristiano ^b,c   Zanacchi, Francesca Cella ^a   Diaspro, Alberto ^a   Gärtner, Wolfgang ^d  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF PARMA   (Italy)

^c ISTITUTO NANOSCIENZE CNR   (Italy)

^d MAX PLANCK INSTITUTE FOR CHEMICAL ENERGY CONVERSION   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MUTANT PROTEIN; UNCLASSIFIED DRUG; VISUAL PROTEINS AND PIGMENTS; YTVA PROTEIN; BACTERIAL PROTEIN; WATER;

ARTICLE; BACILLUS SUBTILIS; CONTROLLED STUDY; DARKNESS; ESCHERICHIA COLI; FLUORESCENCE; HUMIDITY; HYDRATION; HYDROGEN BOND; NONHUMAN; PHOTODYNAMICS; WATER CONTENT; CHEMISTRY; DESICCATION; KINETICS; LIGHT; PHOTOCHEMISTRY; PHYSIOLOGY;

BACTERIA (MICROORGANISMS);

BACILLUS SUBTILIS; BACTERIAL PROTEINS; DESICCATION; KINETICS; LIGHT; PHOTOCHEMICAL PROCESSES; PHOTORECEPTORS, MICROBIAL; WATER;

EID: 84922647236     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107489     Document Type: Article

References (43)

1. Losi A, Polverini E, Quest B, Gärtner W (2002) First evidence for phototropinrelated blue-light receptors in prokaryotes. Biophys J 82: 2627-2634.
2. Gaidenko T, Kim T, Weigel A, Brody M, Price C (2006) The blue-light receptor YtvA acts in the environmental stress signaling pathway of Bacillus subtilis. J Bacteriol 188: 6387-6395.
3. Salomon M, Christie JM, Knieb E, Lempert U, Briggs WR (2000) Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor phototropin. Biochemistry 39: 9401-9410.
4. Losi A (2007) Flavin-based Blue-light Photosensors: A photobiophysics update. PhotochemPhotobiol 83: 1-18.
5. Losi A, Gärtner W, Raffelberg S, Zanacchi FC, Bianchini P, et al. (2013) A photochromic bacterial photoreceptor with potential for super-resolution microscopy. Photochem Photobiol Sci 12: 231-235.
6. Betzig E, Patterson GH, Sougrat R, Lindwasser W, Olenych S, et al. (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313: 1642-1645.
7. Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 3: 793-795.
8. Hess ST, Girirajan TPK, Mason MD (2006) Ultra-high resolution imaging by Fluorescence Photoactivation Localization Microscopy. Biophys J 91: 4258-4272.
9. Raffelberg S, Mansurova M, Gä rtner W, Losi A (2011) Modulation of the photocycle of a LOV domain photoreceptor by the hydrogen bonding network. J Am Chem Soc 133: 5346-5356.
10. Raffelberg S, Gutt A, Gä rtner W, Mandalari C, Abbruzzetti S, et al. (2013) The amino acids surrounding the flavin 7a-methyl group determine the UVA spectral features of a LOV protein. Biol Chem 394: 1517-1528.
11. Zayner JP, Sosnick TR (2014) Factors that control the chemistry of the LOV domain photocycle. PLoS ONE 9: e87074.
12. Kawano F, Aono Y, Suzuki H, Sato M (2013) Fluorescence imaging-based highthroughput screening of fast-and slow-cycling LOV proteins. PLoS ONE 8: e82693.
13. Christie JM, Corchnoy SB, Swartz TE, Hokenson M, Han I-S, et al. (2007) Steric interactions stabilize the signaling state of the LOV2 domain of phototropin 1. Biochemistry 46: 9310-9319.
14. Librizzi F, Viappiani C, Abbruzzetti S, Cordone L (2002) Residual water modulates the dynamics of the protein and of the external matrix in "trehalose coated" MbCO: an infrared and flash photolysis study. J Chem Phys 116: 1193-1200.
15. Palazzo G, Mallardi A, Hochkoeppler A, Cordone L, Venturoli G (2002) Electron transfer kinetics in photosynthetic reaction centers embedded in trehalose glasses: trapping of conformational substates at room temperature. Biophys J 82: 558-568.
16. Giuffrida S, Cottone G, Librizzi F, Cordone L (2003) Coupling between the thermal evolution of the heme pocket and the external matrix structure in trehalose coated carboxymyoglobin. J Phys Chem B 107: 13211-13217.
17. Cordone L, Cottone G, Giuffrida S, Palazzo G, Venturoli G, et al. (2005) Internal dynamics and protein-matrix coupling in trehalose-coated proteins. Biochim Biophys Acta-Proteins and Proteomics 1749: 252-281.
18. Abbruzzetti S, Giuffrida S, Sottini S, Viappiani C, Cordone L (2005) Lightinduced protein-matrix uncoupling and protein relaxation in dry samples of trehalose coated MbCO at room temperature. Cell Biochem Biophys 43: 431-438.
19. Frauenfelder H, Fenimore PW, McMahon BH (2002) Hydration, slaving and protein function. Biophys Chem 98: 35-48.
20. Frauenfelder H, Chen G, Berendzen J, Fenimore PW, Jansson H, et al. (2009) A unified model of protein dynamics. Proc Natl Acad Sci USA 106: 5129-5134.
21. Zoltowski BD, Schwerdtfeger C, Widom J, Loros JJ, Bilwes AM, et al. (2007) Conformational switching in the fungal light sensor vivid. Science 316: 1054-1057.
22. Zoltowski BD, Vaccaro B, Crane BR (2009) Mechanism-based tuning of a LOV domain photoreceptor. Nat Chem Biol 5: 827-834.
23. Alexandre MTA, van Grondelle R, Hellingwerf KJ, Kennis JTM (2009) Conformational heterogeneity and propagation of structural changes in the LOV2 domain from Avena sativa phototropin 1 as recorded by temperaturedependent FTIR Spectroscopy. Biophys J 97: 238-247.
24. Alexandre MTA, Arents JC, van Grondelle R, Hellingwerf KJ, Kennis JTM (2007) A base-catalyzed mechanism for dark state recovery in the Avena sativa phototropin-1 LOV2 Domain. Biochemistry 46: 3129-3137.
25. Laan W, Gauden M, Yeremenko S, van Grondelle R, Kennis JTM, et al. (2005) On the mechanism of activation of the BLUF domain of AppA. Biochemistry 45: 51-60.
26. Chan RH, Lewis JW, Bogomolni RA (2013) Photocycle of the LOV-STAS Protein from the pathogen Listeria monocytogenes. PhotochemPhotobiol 89: 361-369.
27. Fedorov R, Schlichting I, Hartmann E, Domratcheva T, Fuhrmann M, et al. (2003) Crystal structures and molecular mechanism of a light-induced signaling switch: the phot-LOV1 Domain from Chlamydomonas reinhardtii. Biophys J 84: 2474-2482.
28. Genick UK, Soltis SM, Kuhn P, Canestrelli IL, Getzoff ED (1998) Structure at 0.85 A resolution of an early protein photocycle intermediate. Nature 392: 206-209.
29. Key J, Hefti M, Purcell EB, Moffat K (2007) Structure of the redox sensor domain of Azotobacter vinelandii NifL at atomic resolution: signaling, dimerization, and mechanism. Biochemistry 46: 3614-3623.
30. Mandalari C, Losi A, Gartner W (2013) Distance-tree analysis, distribution and co-presence of bilin-and flavin-binding prokaryotic photoreceptors for visible light. Photochemical & Photobiological Sciences 12: 1144-1157.
31. Freddolino PL, Dittrich M, Schulten K (2006) Dynamic switching mechanisms in LOV1 and LOV2 domains of plant phototropins. Biophys J 91: 3630-3639.
32. Zayner JP, Antoniou C, French AR, Hause RJ Jr, Sosnick TR (2013) Investigating models of protein function and allostery with a widespread mutational analysis of a light-activated protein. Biophys J 105: 1027-1036.
33. Zoltowski BD, Nash AI, Gardner KH (2011) Variations in protein-flavin hydrogen bonding in a Light, Oxygen, Voltage domain produce non-Arrhenius kinetics of adduct decay. Biochemistry 50: 8771-8779.
34. Tang Y, Cao Z, Livoti E, Krauss U, Jaeger K-E, et al. (2010) Interdomain signalling in the blue-light sensing and GTP-binding protein YtvA: a mutagenesis study uncovering the importance of specific protein sites. Photochem Photobiol Sci 9: 47-56.
35. Möglich A, Moffat K (2007) Structural basis for light-dependent signaling in the dimeric LOV domain of the photosensor YtvA. J Mol Biol 373: 112-126.
36. Losi A, Kottke T, Hegemann P (2004) Recording of blue light-induced energy and volume changes within the wild-type and mutated phot-LOV1 Domain from Chlamydomonas reinhardtii. Biophys J 86: 1051-1060.
37. Silva-Junior MR, Mansurova M, Gä rtner W, Thiel W (2013) Photophysics of structurally modified flavin derivatives in the blue-light photoreceptor YtvA: a combined experimental and theoretical study. ChemBioChem 14: 1648-1661.
38. Motta-Mena LB, Reade A, Mallory MJ, Glantz S, Weiner OD, et al. (2014) An optogenetic gene expression system with rapid activation and deactivation kinetics. Nat Chem Biol 10: 196-202.
39. Pathak GP, Vrana JD, Tucker CL (2012) Optogenetic control of cell function using engineered photoreceptors. Biology of the Cell 105: 59-72.
40. Schmidt D, Tillberg PW, Chen F, Boyden ES (2014) A fully genetically encoded protein architecture for optical control of peptide ligand concentration. Nat Commun 5.
41. Ellis RJ (2001) Macromolecular crowding: obvious but underappreciated. TIBS 26: 597-604.
42. Ellis RJ (2001) Macromolecular crowding: an important but neglected aspect of the intracellular environment. Curr Opin Struct Biol 11: 114-119.
43. Minton AP (2001) The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J Biol Chem 276: 10577-10580.