Ubiquitous Structural Signaling in Bacterial Phytochromes

Björling, Alexander; Berntsson, Oskar; Takala, Heikki; Gallagher, Kevin D.; Patel, Hardik J.; Gustavsson, Emil; Peter, Rachael St.; Duong, Phu; Nugent, A.C.; Zhang, Fan; Berntsen, Peter; Appio, Roberto; Rajković, Ivan; Lehtivuori, Heli; Panman, Matthijs R.; Hoernke, Maria; Niebling, Stephan; Harimoorthy, Rajiv; Lamparter, Tilman; Stojković, Emina A.; Ihalainen, Janne A.; Westenhoff, Sebastian

doi:10.1021/acs.jpclett.5b01629

Cited by 27 publications

(41 citation statements)

References 41 publications

(72 reference statements)

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“…This shows that the DrBphP PSM is principally capable of controlling both histidine kinase and phosphatase activities in dependence of light. Consistent with this observation, the well-studied conformational changes of the DrBphP PSM during the Pr-to-Pfr transition 26,29,55 are generally very similar across various phytochromes 38 , indicating that both histidine kinase and phosphatase modules can be controlled with other phytochrome photosensory modules.…”

Section: The Bacteriophytochrome From D Radiodurans Is a Light-activsupporting

confidence: 61%

“…Intriguingly, DrBphP lacked autokinase or phosphotransfer activities both in the Pr and Pfr state ( Figure 3A). The absence of kinase activity is surprising as the DrBphP and its PSM evidently undergo light-induced structural changes that seem to be conserved among other phytochromes 29,38,39 . All homologous bacteriophytochrome HKs studied to date exhibited light-dependent kinase activity.…”

Section: Agp1 Functions As a Histidine Kinase But Drbphp Acts As A Phmentioning

confidence: 99%

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Illuminating a Phytochrome Paradigm – a Light-Activated Phosphatase in Two-Component Signaling Uncovered

Multamäki

Nanekar

Morozov

et al. 2020

Preprint

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Bacterial phytochrome photoreceptors usually belong to two-component signaling systems which transmit environmental stimuli to a response regulator through a histidine kinase domain. Phytochromes switch between red light-absorbing and far-red light-absorbing states. Despite exhibiting extensive structural responses during this transition, the model bacteriophytochrome from Deinococcus radiodurans (DrBphP) lacks detectable kinase activity. Here, we resolve this longstanding conundrum by comparatively analyzing the interactions and output activities of DrBphP and a bacteriophytochrome from Agrobacterium fabrum (AgP1). Whereas AgP1 acts as a conventional histidine kinase, we identify DrBphP as a light-sensitive phosphatase. While AgP1 binds its cognate response regulator only transiently, DrBphP does so strongly, which is rationalized at the structural level. Our data pinpoint two key residues affecting the balance between kinase and phosphatase activities, which immediately bears on photoreception and two-component signaling. The opposing output activities in two highly similar bacteriophytochromes inform the use of light-controllable histidine kinases and phosphatases for optogenetics. radiodurans (DrBphP), light induces extensive structural changes in the photosensory module that are relayed to the output module 29 .In terms of enzymatic activity, the dark-adapted Pr state exhibited higher kinase activity than the Pfr state in cyanobacterial phytochrome Cph1, 27,30,31 , similar to other bacteriophytochromes 32 . In particular, the bacteriophytochrome from Agrobacterium fabrum (AgP1) displays histidine kinase activity in its resting Pr state 28,33 ; in the Pfr state, the autophosphorylation and phosphotransfer reactions are down-regulated by 2-fold and 10-fold, respectively 28 . This kinase activity of the AgP1 has been shown to control bacterial conjugation 34 . By contrast, no kinase activity has been demonstrated for DrBphP, notwithstanding close sequence homology and the elaborate structural changes this receptor undergoes under light 22,29 . Despite the eminent role of DrBphP as a paradigm for photoreception, the enzymatic activity and the physiological role of this model phytochrome have hence remained enigmatic.Here, we unravel this long-standing puzzle by studying the enzymatic activity and interactions of DrBphP and AgP1, as two canonical bacteriophytochromes with HK effector domains. By pursuing an integrated biochemical and structural strategy, we show that despite close homology, AgP1 acts as a histidine kinase whereas DrBphP functions as a light-activated phosphatase. Our biochemical and structural data pinpoint two key residues proximal to the catalytic histidine that affect the balance between the kinase and phosphatase activities. Together, the two phytochromes provide soluble, lightcontrollable systems with opposite activities for the study and application of two-component signaling.

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Section: The Bacteriophytochrome From D Radiodurans Is a Light-activsupporting

confidence: 61%

Section: Agp1 Functions As a Histidine Kinase But Drbphp Acts As A Phmentioning

confidence: 99%

Illuminating a Phytochrome Paradigm – a Light-Activated Phosphatase in Two-Component Signaling Uncovered

Multamäki

Nanekar

Morozov

et al. 2020

Preprint

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“…Millisecond time-resolved X-ray scattering was recorded at the Coherent Small-Angle X-ray Scattering (cSAXS) beamline at the Swiss Light Source as previously described 19 . The station uses a rapid-readout detector to detect the time-evolution of the X-ray scattering signal after reaction initiation with a laser pulse 20 .…”

Section: Methodsmentioning

confidence: 99%

Light-induced structural changes in a monomeric bacteriophytochrome

Takala

Niebling

Berntsson

et al. 2016

Structural Dynamics

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Phytochromes sense red light in plants and various microorganism. Light absorption causes structural changes within the protein, which alter its biochemical activity. Bacterial phytochromes are dimeric proteins, but the functional relevance of this arrangement remains unclear. Here, we use time-resolved X-ray scattering to reveal the solution structural change of a monomeric variant of the photosensory core module of the phytochrome from Deinococcus radiodurans. The data reveal two motions, a bend and a twist of the PHY domain with respect to the chromophore-binding domains. Infrared spectroscopy shows the refolding of the PHY tongue. We conclude that a monomer of the phytochrome photosensory core is sufficient to perform the light-induced structural changes. This implies that allosteric cooperation with the other monomer is not needed for structural activation. The dimeric arrangement may instead be intrinsic to the biochemical output domains of bacterial phytochromes.

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“…The available Pr and Pfr PCM structures, including those of bathy‐BPhys and A. thaliana PhyB, largely conform to the scenario laid out for Dr BPhy. Comparative analyses by X‐ray solution scattering revealed that the light‐induced structural changes within the PCM associated with the Pr → Pfr transition are similar across several BPhys . Hence, it appears likely that the above signaling mechanism generally holds for Phys although it is open to which extent bathy and plant Phys differ.…”

Section: Photosensory Inputmentioning

confidence: 99%

“…Pfr transition are similar across several BPhys. 110 Hence, it appears likely that the above signaling mechanism generally holds for Phys although it is open to which extent bathy and plant Phys differ. With but few exceptions, the PCMs have been structurally elucidated in isolation, that is, as PAS-GAF-PHY constructs without covalently attached C-terminal effector module.…”

Section: Bacteriophytochrome Signalingmentioning

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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Ubiquitous Structural Signaling in Bacterial Phytochromes

Cited by 27 publications

References 41 publications

Illuminating a Phytochrome Paradigm – a Light-Activated Phosphatase in Two-Component Signaling Uncovered

Illuminating a Phytochrome Paradigm – a Light-Activated Phosphatase in Two-Component Signaling Uncovered

Light-induced structural changes in a monomeric bacteriophytochrome

Signal transduction in photoreceptor histidine kinases

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