Structural photoactivation of a full-length bacterial phytochrome

Björling, Alexander; Berntsson, Oskar; Lehtivuori, Heli; Takala, Heikki; Hughes, Ashley J.; Panman, Matthijs R.; Hoernke, Maria; Niebling, Stephan; Henry, Léocadie; Henning, Robert; Kosheleva, Irina; Chukharev, Vladimir; Tkachenko, Nikolai V.; Menzel, Andreas; Newby, Gemma; Khakhulin, Dmitry; Wulff, Michaël; Ihalainen, Janne A.; Westenhoff, Sebastian

doi:10.1126/sciadv.1600920

Cited by 103 publications

(159 citation statements)

References 61 publications

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“…A compellingly similar scenario emerges for the BPhy SHK from D. radiodurans, for which structures of the photosensory core module are available in both the Pr and Pfr states, 99,100 see above. Based on this information and X-ray solution scattering experiments, 154 the overall conformational transitions in the full-length receptor upon going from Pr to Pfr were modeled by molecular dynamics. Strikingly, this analysis revealed a light-induced global twist of the receptor as well, albeit of larger extent (around 50 0 ) and of opposite direction, that is, a right-handed mode when viewed from N-to C-terminus ( Figure 7b).…”

Section: The Dynamics Of α-Helical Coiled Coilsmentioning

confidence: 99%

Signal transduction in photoreceptor histidine kinases

Möglich

2019

Protein Science

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Two‐component systems (TCS) constitute the predominant means by which prokaryotes read out and adapt to their environment. Canonical TCSs comprise a sensor histidine kinase (SHK), usually a transmembrane receptor, and a response regulator (RR). In signal‐dependent manner, the SHK autophosphorylates and in turn transfers the phosphoryl group to the RR which then elicits downstream responses, often in form of altered gene expression. SHKs also catalyze the hydrolysis of the phospho‐RR, hence, tightly adjusting the overall degree of RR phosphorylation. Photoreceptor histidine kinases are a subset of mostly soluble, cytosolic SHKs that sense light in the near‐ultraviolet to near‐infrared spectral range. Owing to their experimental tractability, photoreceptor histidine kinases serve as paradigms and provide unusually detailed molecular insight into signal detection, decoding, and regulation of SHK activity. The synthesis of recent results on receptors with light‐oxygen‐voltage, bacteriophytochrome and microbial rhodopsin sensor units identifies recurring, joint signaling strategies. Light signals are initially absorbed by the sensor module and converted into subtle rearrangements of α helices, mostly through pivoting and rotation. These conformational transitions propagate through parallel coiled‐coil linkers to the effector unit as changes in left‐handed superhelical winding. Within the effector, subtle conformations are triggered that modulate the solvent accessibility of residues engaged in the kinase and phosphatase activities. Taken together, a consistent view of the entire trajectory from signal detection to regulation of output emerges. The underlying allosteric mechanisms could widely apply to TCS signaling in general.

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Section: The Dynamics Of α-Helical Coiled Coilsmentioning

confidence: 99%

Signal transduction in photoreceptor histidine kinases

Möglich

2019

Protein Science

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“…The underlying molecular events start with the photoisomerisation of the C ‐ D methine bridge double bond to afford the Lumi intermediates with the chromophore in a highly tensed geometry, followed by thermal relaxation of the chromophore and the immediate protein environment, leading to the formation of the Meta intermediates on the microsecond time scale. The subsequent decay to the final product of the Pr→Pfr (Pfr→Pr) photoconversion involves proton translocation steps in the chromophore pocket and a α‐helix (Pfr) and β‐sheet (Pr) transition in the tongue region of the PHY domain, thought to be functional for (de)activating the downstream signaling chain …”

Section: Figurementioning

confidence: 99%

“… Schematic representation of the photoinduced reaction sequences of phytochromes . The first step refers to the double bond photoisomerization of the ZZZssa (top inset) and ZZEssa configuration (bottom inset) in Pr and Pfr, respectively (the C‐D methine bridge and ring D are highlighted in red).…”

Section: Figurementioning

confidence: 99%

The Photoconversion of Phytochrome Includes an Unproductive Shunt Reaction Pathway

et al. 2018

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Phytochromes are modular bimodal photoswitches that control gene expression for morphogenetic processes in plants. These functions are triggered by photoinduced conversions between the inactive and active states of the photosensory module, denoted as Pr and Pfr, respectively. In the present time-resolved resonance Raman spectroscopic study of bacterial representatives of this photoreceptor family, we demonstrate that these phototransformations do not represent linear processes but include a branching reaction back to the initial state, prior to (de)activation of the output module. Thus, only a fraction of the photoreceptors undergoing the phototransformations can initiate the downstream signaling process, consistent with phytochrome's function as a sensor for more durable changes of light conditions.

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“…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).…”

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confidence: 99%

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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Structural photoactivation of a full-length bacterial phytochrome

Abstract: Time-resolved x-ray solution scattering reveals the conformational signaling mechanism of a bacterial phytochrome.

Cited by 103 publications

References 61 publications

Signal transduction in photoreceptor histidine kinases

Signal transduction in photoreceptor histidine kinases

The Photoconversion of Phytochrome Includes an Unproductive Shunt Reaction Pathway

Signaling mechanism of phytochromes in solution

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