Ground-state heterogeneity and vibrational energy redistribution in bacterial phytochrome observed with femtosecond 2D IR spectroscopy
(2023) In Journal of Chemical Physics 158(8).- Abstract
Phytochromes belong to a group of photoreceptor proteins containing a covalently bound biliverdin chromophore that inter-converts between two isomeric forms upon photoexcitation. The existence and stability of the photocycle products are largely determined by the protein sequence and the presence of conserved hydrogen-bonding interactions in the vicinity of the chromophore. The vibrational signatures of biliverdin, however, are often weak and obscured under more intense protein bands, limiting spectroscopic studies of its non-transient signals. In this study, we apply isotope-labeling techniques to isolate the vibrational bands from the protein-bound chromophore of the bacterial phytochrome from Deinococcus radiodurans. We elucidate the... (More)
Phytochromes belong to a group of photoreceptor proteins containing a covalently bound biliverdin chromophore that inter-converts between two isomeric forms upon photoexcitation. The existence and stability of the photocycle products are largely determined by the protein sequence and the presence of conserved hydrogen-bonding interactions in the vicinity of the chromophore. The vibrational signatures of biliverdin, however, are often weak and obscured under more intense protein bands, limiting spectroscopic studies of its non-transient signals. In this study, we apply isotope-labeling techniques to isolate the vibrational bands from the protein-bound chromophore of the bacterial phytochrome from Deinococcus radiodurans. We elucidate the structure and ultrafast dynamics of the chromophore with 2D infra-red (IR) spectroscopy and molecular dynamics simulations. The carbonyl stretch vibrations of the pyrrole rings show the heterogeneous distribution of hydrogen-bonding structures, which exhibit distinct ultrafast relaxation dynamics. Moreover, we resolve a previously undetected 1678 cm-1 band that is strongly coupled to the A- and D-ring of biliverdin and demonstrate the presence of complex vibrational redistribution pathways between the biliverdin modes with relaxation-assisted measurements of 2D IR cross peaks. In summary, we expect 2D IR spectroscopy to be useful in explaining how point mutations in the protein sequence affect the hydrogen-bonding structure around the chromophore and consequently its ability to photoisomerize to the light-activated states.
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- author
- Chenchiliyan, Manoop LU ; Kübel, Joachim ; Ooi, Saik Ann ; Salvadori, Giacomo ; Mennucci, Benedetta ; Westenhoff, Sebastian LU and Maj, Michał
- publishing date
- 2023-02-28
- type
- Contribution to journal
- publication status
- published
- subject
- in
- Journal of Chemical Physics
- volume
- 158
- issue
- 8
- article number
- 085103
- publisher
- American Institute of Physics (AIP)
- external identifiers
-
- pmid:36859103
- scopus:85149113027
- ISSN
- 0021-9606
- DOI
- 10.1063/5.0135268
- language
- English
- LU publication?
- no
- additional info
- Publisher Copyright: © 2023 Author(s).
- id
- 28413a76-8ac6-42ad-bcda-cf8c2d2e05a6
- date added to LUP
- 2023-06-16 10:31:32
- date last changed
- 2024-04-19 22:52:56
@article{28413a76-8ac6-42ad-bcda-cf8c2d2e05a6,
abstract = {{<p>Phytochromes belong to a group of photoreceptor proteins containing a covalently bound biliverdin chromophore that inter-converts between two isomeric forms upon photoexcitation. The existence and stability of the photocycle products are largely determined by the protein sequence and the presence of conserved hydrogen-bonding interactions in the vicinity of the chromophore. The vibrational signatures of biliverdin, however, are often weak and obscured under more intense protein bands, limiting spectroscopic studies of its non-transient signals. In this study, we apply isotope-labeling techniques to isolate the vibrational bands from the protein-bound chromophore of the bacterial phytochrome from Deinococcus radiodurans. We elucidate the structure and ultrafast dynamics of the chromophore with 2D infra-red (IR) spectroscopy and molecular dynamics simulations. The carbonyl stretch vibrations of the pyrrole rings show the heterogeneous distribution of hydrogen-bonding structures, which exhibit distinct ultrafast relaxation dynamics. Moreover, we resolve a previously undetected 1678 cm-1 band that is strongly coupled to the A- and D-ring of biliverdin and demonstrate the presence of complex vibrational redistribution pathways between the biliverdin modes with relaxation-assisted measurements of 2D IR cross peaks. In summary, we expect 2D IR spectroscopy to be useful in explaining how point mutations in the protein sequence affect the hydrogen-bonding structure around the chromophore and consequently its ability to photoisomerize to the light-activated states.</p>}},
author = {{Chenchiliyan, Manoop and Kübel, Joachim and Ooi, Saik Ann and Salvadori, Giacomo and Mennucci, Benedetta and Westenhoff, Sebastian and Maj, Michał}},
issn = {{0021-9606}},
language = {{eng}},
month = {{02}},
number = {{8}},
publisher = {{American Institute of Physics (AIP)}},
series = {{Journal of Chemical Physics}},
title = {{Ground-state heterogeneity and vibrational energy redistribution in bacterial phytochrome observed with femtosecond 2D IR spectroscopy}},
url = {{http://dx.doi.org/10.1063/5.0135268}},
doi = {{10.1063/5.0135268}},
volume = {{158}},
year = {{2023}},
}