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Cited by 183Electromagnetic Fields and Biological EffectsElectron Spin Resonance StudiesCircadian rhythm and melatonin

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Chemical Magnetoreception: Bird Cryptochrome 1a Is Excited by Blue Light and Forms Long-Lived Radical-Pairs

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Liedvogel, Miriam, Maeda, Kiminori, Henbest, Kevin, Schleicher, Erik, Simon, Thomas, Timmel, Christiane R., Hore, P. J., Mouritsen, Henrik·2007·PLoS ONE
DOI 10.1371/journal.pone.0001106PMC PMC2040520
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Abstract

Cryptochromes (Cry) have been suggested to form the basis of light-dependent magnetic compass orientation in birds. However, to function as magnetic compass sensors, the cryptochromes of migratory birds must possess a number of key biophysical characteristics. Most importantly, absorption of blue light must produce radical pairs with lifetimes longer than about a microsecond. Cryptochrome 1a (gwCry1a) and the photolyase-homology-region of Cry1 (gwCry1-PHR) from the migratory garden warbler were recombinantly expressed and purified from a baculovirus/Sf9 cell expression system. Transient absorption measurements show that these flavoproteins are indeed excited by light in the blue spectral range leading to the formation of radicals with millisecond lifetimes. These biophysical characteristics suggest that gwCry1a is ideally suited as a primary light-mediated, radical-pair-based magnetic compass receptor.

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Figures

Figure 1 Transient absorption spectra for gwCry1a. A Transient absorption spectra for gwCry1a as a function of wavelength (monitoring beam) proves that radical pairs are produced in cryptochromes of a migratory bird. The five graphs reflect the optical properties of the sample at different times, t delay, after the laser flash. The amplitude of the signals depends on the protein concentration. The spectra were obtained by averaging two time profiles (cf. Fig. 1B) centred at t delay using a time window of 500 µs. The variation of the absorption signal is about 5%, which is estimated from the data at 0.5 ms from 500 to 600 nm. For a detailed analysis of the spectra, see main text. B Transient absorption time profiles for gwCry1a. A laser flash (indicated by the arrow) is given at time = 0. The transient signal is obtained by averaging 7 time-profiles for the 490–550 nm wavelength region (corresponding to the optical features framed in blue in Fig. 1A) in 10 nm steps (blue curve, left scale) and 9 time-profiles for the 550–630 nm region (corresponding to the optical features framed in red in Fig. 1A) in 10 nm steps (red, graph, right scale), respectively. Solid lines show the fitted single or double exponential decays. The laser flash leads to radical formation as reflected by positive changes in the absorption signal. Significant radical concentrations are detectable up to ∼25 ms. For further discussion, see main text.
Figure 1 Transient absorption spectra for gwCry1a. A Transient absorption spectra for gwCry1a as a function of wavelength (monitoring beam) proves that radical pairs are produced in cryptochromes of a migratory bird. The five graphs reflect the optical properties of the sample at different times, t delay, after the laser flash. The amplitude of the signals depends on the protein concentration. The spectra were obtained by averaging two time profiles (cf. Fig. 1B) centred at t delay using a time window of 500 µs. The variation of the absorption signal is about 5%, which is estimated from the data at 0.5 ms from 500 to 600 nm. For a detailed analysis of the spectra, see main text. B Transient absorption time profiles for gwCry1a. A laser flash (indicated by the arrow) is given at time = 0. The transient signal is obtained by averaging 7 time-profiles for the 490–550 nm wavelength region (corresponding to the optical features framed in blue in Fig. 1A) in 10 nm steps (blue curve, left scale) and 9 time-profiles for the 550–630 nm region (corresponding to the optical features framed in red in Fig. 1A) in 10 nm steps (red, graph, right scale), respectively. Solid lines show the fitted single or double exponential decays. The laser flash leads to radical formation as reflected by positive changes in the absorption signal. Significant radical concentrations are detectable up to ∼25 ms. For further discussion, see main text.CC BY · PubMed Central
Figure 2 SDS-PAGE of recombinantly expressed garden warbler cryptochrome (shown for gwCry1a protein). A Coomassie stained SDS gel, and B Western-blot (with α-Cry1 antiserum from immunised goat), both showing identical fractions of the IMAC purification process. gwCry1a (628 aa) is recognisable as a distinct band at ∼62 kDa in both the coomassie stained SDS gel and on the Western-blot (indicated by the arrowhead to the right). 1: gwCry1a lysate (protein extract from insect cell pellet, 1∶10 dilution); 2: gwCry1a cleared lysate (centrifuged and filtered lysate, 1∶10 dilution); 3: gwCry1a flow through (after sample loading on column, 1∶10 dilution); 4: gwCry1a elution step1 (e1) [75% imidazole]; 5: gwCry1a elution step2 (e2) [100% imidazole] protein quantity for e2 is 5 µg; 6: negative control (recombinantly expressed human La/SSB autoantigen; ∼48 kDa) confirms the specificity of the antibody.
Figure 2 SDS-PAGE of recombinantly expressed garden warbler cryptochrome (shown for gwCry1a protein). A Coomassie stained SDS gel, and B Western-blot (with α-Cry1 antiserum from immunised goat), both showing identical fractions of the IMAC purification process. gwCry1a (628 aa) is recognisable as a distinct band at ∼62 kDa in both the coomassie stained SDS gel and on the Western-blot (indicated by the arrowhead to the right). 1: gwCry1a lysate (protein extract from insect cell pellet, 1∶10 dilution); 2: gwCry1a cleared lysate (centrifuged and filtered lysate, 1∶10 dilution); 3: gwCry1a flow through (after sample loading on column, 1∶10 dilution); 4: gwCry1a elution step1 (e1) [75% imidazole]; 5: gwCry1a elution step2 (e2) [100% imidazole] protein quantity for e2 is 5 µg; 6: negative control (recombinantly expressed human La/SSB autoantigen; ∼48 kDa) confirms the specificity of the antibody.CC BY · PubMed Central
Figure 3 Optical spectroscopy of cryptochrome holoprotein from migratory garden warblers. A gwCry1-PHR, illumination time: 0 s (black), 40 s (yellow), 80 s (orange), 130 s (light blue), 190 s (blue) and 340 s (green), respectively. B gwCry1a, illumination time: 0 s (black), 90 s (yellow), 150 s (orange), 240 s (light blue), 360 s (blue) and 540 s (green), respectively. Both samples were illuminated under anaerobic conditions as indicated in the Methods section. Reoxidation was achieved by bubbling air into the optical cuvette (red dashed lines).
Figure 3 Optical spectroscopy of cryptochrome holoprotein from migratory garden warblers. A gwCry1-PHR, illumination time: 0 s (black), 40 s (yellow), 80 s (orange), 130 s (light blue), 190 s (blue) and 340 s (green), respectively. B gwCry1a, illumination time: 0 s (black), 90 s (yellow), 150 s (orange), 240 s (light blue), 360 s (blue) and 540 s (green), respectively. Both samples were illuminated under anaerobic conditions as indicated in the Methods section. Reoxidation was achieved by bubbling air into the optical cuvette (red dashed lines).CC BY · PubMed Central
Figure 4 Sequence alignment between different members and species within the cryptochrome/photolyase protein family. A Sequence alignment of Cry1a of two migratory songbird species Sylvia borin (Garden warbler; GenBank accession no. AJ632120), Erithacus rubecula (European robin; AY585716), Cry1 of Arabidopsis thaliana (mouse-ear cress; Q43125) and DNA photolyase of Escherichia coli (P00914). The alignment shows that all three members of the Trp-triad electron transfer chain known to be involved in intraprotein electron transfer during signalling through photoreduction in both E. coli photolyse and AtCry1 are clearly present in the Cry1a sequences of both migratory bird species (Trp-397, Trp-374, Trp-321). B Reaction scheme for gwCry1a (adapted from a very similar scheme for AtCry1 proposed by Giovani et al. [36]). Processes directly observed here are represented by solid arrows. Other steps are indicated by dashed arrows [36]. The excited state of the FAD is assumed here to be a singlet; an almost identical scheme would result if, instead, triplet FAD were assumed to be the photoactive excited state. Singlet-triplet interconversion in the [FADH• Trp•] radical pair is indicated by the curved block arrows. D and A are respectively an external electron donor and acceptor.
Figure 4 Sequence alignment between different members and species within the cryptochrome/photolyase protein family. A Sequence alignment of Cry1a of two migratory songbird species Sylvia borin (Garden warbler; GenBank accession no. AJ632120), Erithacus rubecula (European robin; AY585716), Cry1 of Arabidopsis thaliana (mouse-ear cress; Q43125) and DNA photolyase of Escherichia coli (P00914). The alignment shows that all three members of the Trp-triad electron transfer chain known to be involved in intraprotein electron transfer during signalling through photoreduction in both E. coli photolyse and AtCry1 are clearly present in the Cry1a sequences of both migratory bird species (Trp-397, Trp-374, Trp-321). B Reaction scheme for gwCry1a (adapted from a very similar scheme for AtCry1 proposed by Giovani et al. [36]). Processes directly observed here are represented by solid arrows. Other steps are indicated by dashed arrows [36]. The excited state of the FAD is assumed here to be a singlet; an almost identical scheme would result if, instead, triplet FAD were assumed to be the photoactive excited state. Singlet-triplet interconversion in the [FADH• Trp•] radical pair is indicated by the curved block arrows. D and A are respectively an external electron donor and acceptor.CC BY · PubMed Central

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Metadata

Authors
Liedvogel, M., Maeda, K., Henbest, K., Schleicher, E., Simon, T., Timmel, C. R., Hore, P. J., & Mouritsen, H.
Affiliations
  • Carl von Ossietzky Universität Oldenburg (DE)
  • University of Oxford (GB)
  • Freie Universität Berlin (DE)
Corresponding author
  • Liedvogel, Miriam
  • Maeda, Kiminori
  • Henbest, Kevin
  • Schleicher, Erik
  • Simon, Thomas
  • Timmel, Christiane R.
  • Hore, P. J.
  • Mouritsen, Henrik
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2007-10-31
Volume
2
Issue
10
Pages
e1106
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0001106
PMC
PMC2040520
OpenAlex
W2163169468
Cited by
183
References
54
Citations by year
2026: 3 · 2025: 7 · 2024: 7 · 2023: 6 · 2022: 7 · 2021: 11 · 2020: 9 · 2019: 3 · 2018: 12 · 2017: 12 · 2016: 14 · 2015: 11 · 2014: 11 · 2013: 8 · 2012: 11
FWCI
7.68
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Max Planck Digital Library (submittedVersion, other-oa)
  • Figshare (submittedVersion, cc-by)
  • Lund University Publications (Lund University) (submittedVersion)
  • Refubium (Universitätsbibliothek der Freien Universität Berlin) (submittedVersion, cc-by)
Funders
  • Carl von Ossietzky Universität Oldenburg
  • Royal Society
  • EMF Biological Research Trust
  • Deutsche Forschungsgemeinschaft (FOR 526, MO 1408/1-2, FOR 701)
  • Volkswagen Foundation
  • Engineering and Physical Sciences Research Council (GR/T05424/01)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Electromagnetic Fields and Biological Effects
  • Physical Sciences › Chemistry › Spectroscopy › Electron Spin Resonance Studies
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
Keywords
radical pairs, blue light absorption, flavoprotein, magnetic compass orientation, bird migration, garden warbler, transient absorption spectroscopy, recombinant protein expression
MeSH terms
Animals, Birds, Cell Line, Cloning, Molecular, Flavoproteins, Free Radicals, Insecta, Light, Magnetics, Models, Biological, Magnetic Resonance Spectroscopy, Recombinant Proteins, Ultraviolet Rays, Protein Structure, Tertiary, Animal Migration, Cryptochromes

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