Light-induced structural changes in a monomeric bacteriophytochrome

Takala, Heikki; Niebling, Stephan; Berntsson, Oskar; Björling, Alexander; Lehtivuori, Heli; Häkkänen, Heikki; Panman, Matthijs R.; Gustavsson, Emil; Hoernke, Maria; Newby, Gemma; Zontone, Federico; Wulff, Michaël; Menzel, Andreas; Ihalainen, Janne A.; Westenhoff, Sebastian

doi:10.1063/1.4961911

Cited by 40 publications

(57 citation statements)

References 47 publications

(63 reference statements)

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“…This would be consistent with structural changes, refined against time-resolved X-ray scattering data for Dr BphP mon and for the full length Dr BphP. 27,28 The studies identified a twist and bending of the photosensory core 27 and an overall twist of the output domains with respect to PAS/GAF. 28 This is also consistent with how other sensory proteins are thought to work.…”

Section: Discussionsupporting

confidence: 64%

“…This indicates that the quaternary structure of Dr BphP mon is not changed dramatically upon photoactivation, which is consistent with the time-resolved solution scattering structures of the same protein fragment. 27 We also determined 15 N T1 and T2 relaxation times for each residue (Fig. 3a, b and SI Appendix, Fig.…”

Section: Residual Dipolar Couplings (Rdc) Indicate Changes In the Knomentioning

confidence: 99%

“…The knot in group I phytochromes is formed at the interface between the PAS and GAF domains spanning the space between the chromophore and the helical spine (residue [27][28][29][30][31][32][33][34][35][36][37][38] and 228-256) ( Fig. 1a).…”

mentioning

confidence: 99%

“…1a). 7 The sequence between Cys24 and the start of the PAS domain (residue [27][28][29][30][31][32][33][34][35][36][37][38] is passed through a loop formed by a large insertion within the GAF domain (residue 228-256). 7 The knot is stabilized by a small but critical hydrophobic core, centered on the conserved Ile35.…”

mentioning

confidence: 99%

“…18,26 A bending of the spine in between the PAS-GAF and PHY domains has been inferred from crystal structures, X-ray solution scattering, and DEER spectroscopy (SI Appendix, Fig. S2a), 16,21,[27][28][29] but more detailed changes in the spine have not been reported.…”

mentioning

confidence: 99%

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Signaling mechanism of phytochromes in solution

Isaksson

Gustavsson

Persson

et al. 2020

Preprint

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Phytochrome proteins guide the red/far-red photoresponse of plants, fungi, and bacteria. The proteins change their structure in response to light, thereby altering their biochemical activity. Crystal structures suggest that the mechanism of signal transduction involves refolding of the so-called PHY tongue, but the two other notable structural features of the phytochrome superfamily, the helical spine and a figure-ofeight knot, have not been implied in the signaling mechanism. Here, we present solution NMR data of the complete photosensory core module from D. radiodurans (Dr BphP). Photoswitching between the resting and active states induces changes in amide chemicalshifts, residual dipolar couplings, and relaxation dynamics. All observables indicate a photoinduced structural change in the knot region and lower part of the helical spine.Supported by functional studies of plant phytochromes, the new mechanism explains how the conformational signal is directed through the protein to the signaling spine.The new pathway explains photo-sensing by phytochromes with atomic precision under biological conditions.Phytochromes are universal photoreceptors found in plants, fungi, and various microorganisms. 1 They detect red and far-red light, thereby controlling many aspects of growth, development, and movement. The functions range from phototaxis and pigmentation in bacteria to seed germination, shade avoidance and flowering in higher plants. [2][3][4][5][6][7][8] Phytochromes work by switching between two photochemical states. In prototypical phytochromes, the resting state absorbs red light (Pr state), and the activated state absorbs far-red light (Pfr state).The proteins can be reversibly switched between the states with red light (Pr→Pfr) and farred light (Pfr→Pr). Phytochromes are important for life, since they ensure that microbes and vegetation can adapt to light and thrive on earth.Similar to other signaling proteins, 9,10 phytochromes are modular proteins. They are divided into three groups according to the domain architecture. Group I phytochromes share a highly conserved photosensory module consisting of the domains PAS-GAF-PHY (Per/Arndt/Sim-cGMP phosphodiesterase/adenyl cyclase/Fh1A-phytochrome specific). 11,12 Plant, fungal and bacterial phytochromes belong to this group. The photosensory module of the cyanobacterial group II and III phytochromes consist of GAF-PHY and GAF, respectively. 13 A covalently linked bilin chromophore (biliverdin in bacterial phytochromes) is attached via a thioether linkage to a conserved cysteine in the GAF domain (cyanobacteria and plants) or PAS domain (bacteria). 11 Output domains vary and can consists of a C-terminal histidine kinase in bacteria, so-called N-terminal extensions, and C-terminal PAS domains connected to a kinase-like domain in plants and fungi. 12 Phytochromes are usually homodimers.The photosensory module of phytochromes contains three characteristic structural elements. These are a conserved loop region in the PHY domain, called "tongue" (residue 444-476, grou...

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Section: Discussionsupporting

confidence: 64%

Section: Residual Dipolar Couplings (Rdc) Indicate Changes In the Knomentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Signaling mechanism of phytochromes in solution

Isaksson

Gustavsson

Persson

et al. 2020

Preprint

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It's a two‐way street: Photoswitching and reversible changes of the protein matrix in photoswitchable fluorescent proteins and bacteriophytochromes

Rodrigues

Stiel

2023

FEBS Letters

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Chromophore‐bearing proteins that are (reversibly) altered after light illumination are major functional components of nature. They gained considerable attention in the last decades since the dynamic interactions of the chromophore and protein matrix can be used to control downstream effects altering the functionality of proteins, cells, or complete organisms with light (optogenetics). Additionally, the photophysical effects can be employed to add capabilities to optical imaging. For example, light can be used to reversibly switch the signal on or off (e.g., fluorescence). In this article, we review chromophore and protein matrix interactions, focusing on photoswitching fluorescent proteins of the GFP family (RSFPs) and natively photoswitching bacteriophytochromes (BphPs). This review aims to provide an in‐depth understanding of the dynamic interplay between photoswitching photophysics and the protein matrix and a thorough discussion on how this connection has been harnessed for the development of optogenetic and imaging tools.

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The structural effect between the output module and chromophore-binding domain is a two-way street via the hairpin extension

Kurttila

Etzl

Rumfeldt

et al. 2022

Photochem Photobiol Sci

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Signal transduction typically starts with either ligand binding or cofactor activation, eventually affecting biological activities in the cell. In red light-sensing phytochromes, isomerization of the bilin chromophore results in regulation of the activity of diverse output modules. During this process, several structural elements and chemical events influence signal propagation. In our study, we have studied the full-length bacteriophytochrome from Deinococcus radiodurans as well as a previously generated optogenetic tool where the native histidine kinase output module has been replaced with an adenylate cyclase. We show that the composition of the output module influences the stability of the hairpin extension. The hairpin, often referred as the PHY tongue, is one of the central structural elements for signal transduction. It extends from a distinct domain establishing close contacts with the chromophore binding site. If the coupling between these interactions is disrupted, the dynamic range of the enzymatic regulation is reduced. Our study highlights the complex conformational properties of the hairpin extension as a bidirectional link between the chromophore-binding site and the output module, as well as functional properties of diverse output modules.

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Light-induced structural changes in a monomeric bacteriophytochrome

Cited by 40 publications

References 47 publications

Signaling mechanism of phytochromes in solution

Signaling mechanism of phytochromes in solution

It's a two‐way street: Photoswitching and reversible changes of the protein matrix in photoswitchable fluorescent proteins and bacteriophytochromes

The structural effect between the output module and chromophore-binding domain is a two-way street via the hairpin extension

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