Light-induced electron transfer in a cryptochrome blue-light photoreceptor

Giovani, Baldissera; Byrdin, Martin; Ahmad, Margaret; Brettel, Klaus

doi:10.1038/nsb933

Cited by 255 publications

(346 citation statements)

References 15 publications

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“…We stress that the identity of RP2 in AtCry is not crucial for the interpretation of the magnetic-field effects reported below. In light of previous work (9,10,24,28,29), the Trp radicals are presumed to come from the terminal residue of the Trp-triad, i.e. Trp-324 in AtCry and Trp-306 in EcPL.…”

Section: Resultsmentioning

confidence: 99%

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Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor

Maeda

Robinson

Henbest

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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314

480

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Among the biological phenomena that fall within the emerging field of “quantum biology” is the suggestion that magnetically sensitive chemical reactions are responsible for the magnetic compass of migratory birds. It has been proposed that transient radical pairs are formed by photo-induced electron transfer reactions in cryptochrome proteins and that their coherent spin dynamics are influenced by the geomagnetic field leading to changes in the quantum yield of the signaling state of the protein. Despite a variety of supporting evidence, it is still not clear whether cryptochromes have the properties required to respond to magnetic interactions orders of magnitude weaker than the thermal energy, k B T . Here we demonstrate that the kinetics and quantum yields of photo-induced flavin—tryptophan radical pairs in cryptochrome are indeed magnetically sensitive. The mechanistic origin of the magnetic field effect is clarified, its dependence on the strength of the magnetic field measured, and the rates of relevant spin-dependent, spin-independent, and spin-decoherence processes determined. We argue that cryptochrome is fit for purpose as a chemical magnetoreceptor.

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Section: Resultsmentioning

confidence: 99%

“…Photoreduction of the fully oxidized state of FAD in most proteins of the cryptochrome/photolyase family appears to be mediated by electron transfer along a conserved triad of tryptophan (Trp) residues to give a flavosemiquinone radical, FAD •− or FADH • , together with a radical derived from the terminal residue of the Trp-triad (8)(9)(10)(11) (Fig. 1).…”

mentioning

confidence: 99%

Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor

Maeda

Robinson

Henbest

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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314

480

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“…The present results show that the hydrogen-bond switch in BLUF domains is driven by initial ET from aromatic residues to the oxidized flavin. In the cryptochromes, similar ET processes appear to underlie their activity, with Trps as likely electron donors (10,33). The question remains whether in LOV domains, ET or PT from a conserved Cys to the FMN chromophore constitutes the primary photochemical event (9,(34)(35)(36).…”

Section: Light-induced Et: a General Theme In Flavin-binding Photorecmentioning

confidence: 99%

“…In the phototropins, for instance, signaling occurs through the light-induced formation of a covalent adduct between the flavin chromophore and a conserved cysteine in light, oxygen, or voltage (LOV) domains, which eventually leads to autophosphorylation of a C-terminal Ser͞Thr kinase (8,9). In analogy with the related photolyases, cryptochromes are thought to function by means of light-induced electron transfer (ET) reactions (10), but at present their mode of action remains largely obscure.…”

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confidence: 99%

Hydrogen-bond switching through a radical pair mechanism in a flavin-binding photoreceptor

Gauden

Stokkum²,

Key³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

218

435

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BLUF (blue light sensing using FAD) domains constitute a recently discovered class of photoreceptor proteins found in bacteria and eukaryotic algae, where they control a range of physiological responses including photosynthesis gene expression, photophobia, and negative phototaxis. Other than in well known photoreceptors such as the rhodopsins and phytochromes, BLUF domains are sensitive to light through an oxidized flavin rather than an isomerizable cofactor. To understand the physicochemical basis of BLUF domain photoactivation, we have applied femtosecond transient absorption spectroscopy to the Slr1694 BLUF domain of Synechocystis PCC6803. We show that photoactivation of BLUF domains proceeds by means of a radical-pair mechanism, driven by electron and proton transfer from the protein to the flavin, resulting in the transient formation of anionic and neutral flavin radical species that finally result in the long-lived signaling state on a 100-ps timescale. A pronounced deuteration effect is observed on the lifetimes of the intermediate radical species, indicating that proton movements underlie their molecular transformations. We propose a photoactivation mechanism that involves a successive rupture of hydrogen bonds between a conserved tyrosine and glutamine by light-induced electron transfer from tyrosine to flavin and between the glutamine and flavin by subsequent protonation at flavin N5. These events allow a reorientation of the conserved glutamine, resulting in a switching of the hydrogen-bond network connecting the chromophore to the protein, followed by radicalpair recombination, which locks the glutamine in place. It is suggested that the redox potential of flavin generally defines the light sensitivity of flavin-binding photoreceptors.flavoprotein ͉ light sensing ͉ photochemistry ͉ reaction mechanism ͉ spectroscopy

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“…[2][3][4][5] Blue-light excitation of the flavin adenine dinucleotide (FAD) chromophore in cryptochrome is thought to trigger intra-protein electron transfers along a triad of tryptophan (Trp) residues to give a stabilised, charge-separated FAD-Trp radical pair. [6][7][8][9] Transient absorption studies 10 have shown that coherent interconversion of the electronic singlet and triplet states of the radical pair gives rise to long lived states of the protein whose quantum yields can be modified by applied magnetic fields via the well-established radical pair mechanism. 11,12 Studies of the magnetic sensitivity of cryptochromes are currently constrained by the relatively high protein concentrations and large sample volumes required for absorption-based spectroscopy and by the photo-degradation caused by the intense laser pulses often needed for such measurements.…”

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confidence: 99%

Fluorescence-detected magnetic field effects on radical pair reactions from femtolitre volumes

et al. 2015

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We show that the effects of applied magnetic fields on radical pair reactions can be sensitively measured from sample volumes as low as ~100 femtolitres using total internal reflection fluorescence microscopy. Development of a fluorescence-based microscope method is likely to be a key step in further miniaturisation that will allow detection of magnetic field effects on single molecules.Flavins -tricyclic aza-aromatic compounds -occur widely in Nature and perform a variety of biological functions, many of which involve electron transfer. 1 Attention has recently focussed on the flavoprotein cryptochrome which has been proposed as the primary sensory molecule by which migratory birds detect the direction of the Earth's magnetic field. 2-5 Blue-light excitation of the flavin adenine dinucleotide (FAD) chromophore in cryptochrome is thought to trigger intra-protein electron transfers along a triad of tryptophan (Trp) residues to give a stabilised, charge-separated FAD-Trp radical pair. 6-9 Transient absorption studies 10 have shown that coherent interconversion of the electronic singlet and triplet states of the radical pair gives rise to long lived states of the protein whose quantum yields can be modified by applied magnetic fields via the well-established radical pair mechanism. 11,12 Studies of the magnetic sensitivity of cryptochromes are currently constrained by the relatively high protein concentrations and large sample volumes required for absorption-based spectroscopy and by the photo-degradation caused by the intense laser pulses often needed for such measurements. 13,14 Cryptochromes -in particular the vertebrate proteins -are difficult to express recombinantly in large quantities and tend to aggregate in concentrated solution. Further in vitro studies of their magnetic responses will require a detection method compatible with much smaller quantities of protein, the obvious choice being fluorescence.Fluorescence has been used extensively to monitor magnetic field effects (MFEs) on the photochemistry of small organic radicals. In appropriate, usually non-aqueous, solvents singlet but not triplet radical pairs can often recombine to form an exciplex whose fluorescence provides a convenient and sensitive probe of the magnetic response. [15][16][17][18] Effective though such an approach has proved, it is manifestly inapplicable when the radical pair cannot recombine to form a luminescent state. Many radical pairs, including flavin-Trp, do not form excited molecular complexes and cryptochromes have no other electronically excited states that can be populated from the FAD-Trp radical pair.However, flavins do have fluorescent excited states that can be exploited as MFE probes. For cyclic photochemical reactions under conditions of continuous illumination, the fluorescence intensity reflects the steady state concentration of ground state flavin, which in turn depends on the concentrations of long-lived radical intermediates in the photocycle. If all other species are short lived and thus present in low concentra...

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Light-induced electron transfer in a cryptochrome blue-light photoreceptor

Cited by 255 publications

References 15 publications

Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor

Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor

Hydrogen-bond switching through a radical pair mechanism in a flavin-binding photoreceptor

Fluorescence-detected magnetic field effects on radical pair reactions from femtolitre volumes

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