Glycine, an Amino Acid and Other Prebiotic Molecules in Comet 67P/Churyumov-Gerasimenko

Kathrin Altwegg 

Author: Kathrin Altwegg and the ROSINA Team 

Affiliation: Physikalisches Institut, University of Bern, Switzerland.

By now it is an established fact that comets contain the most primitive material of all solar system bodies. In situ results from the Giotto flyby at comet Halley in 1986 and remote sensing in various wavelength ranges established the presence of many organic molecules in the coma of comets. The importance of comets for the origin of life on Earth has been the topic of many discussions in the past [1]. Among the key ingredients for life as we know it are amino acids and phosphorous. Many primitive meteorites contain amino acids. However most of them are formed by aqueous alterations [2,3]. Traces of amino acids were detected in samples from the Stardust mission to comet Wild 2 [4]. However, there always remained some doubts that these amino acids were actually cometary as the extraction and analysis of the material from the aerogel and aluminium frame always involves either hot water or even acids, which could then readily form amino acid on Earth.

In order to investigate the composition of the organics and to assess the importance of comets for the origin of terrestrial life the European Space Agency ESA launched in 2004 the spacecraft Rosetta towards comet 67P/ Churyumov-Gerasimenko . This comet belongs to the Jupiter family with an aphelion at 5.5 AU and a perihelion at 1.25 AU. Its orbital period is 6.5 y. In order to match the comet’s orbit Rosetta had to flyby three times the Earth and once Mars to arrive at the comet more than 10 years after launch in August 2014. Subsequently, Rosetta flew with the comet around the Sun from 3.6 AU to perihelion and out again to 3.8 AU, sometimes as close as 10 km from the comet centre. This allowed a thorough investigation of the comet from up close during the different phases of its orbit.

On board Rosetta was the ROSINA (Rosetta Orbiter Sensor for Ion and Neutral Analysis) suite consisting of two mass spectrometers (DFMS and RTOF) and the cometary pressure sensor COPS [5]. These sensors were built to analyse the composition of the cometary atmosphere along its path around the Sun, encountering very low densities for large heliocentric distances to much more violent outgassing during perihelion.

ROSINA measured almost continuously during more than two years. Most of the time, water was the dominant component of the cometary coma. However, due to its peculiar shape and the tilted rotation axis of the comet, the coma was very heterogeneous and varying along the orbit. Apart from water, ROSINA identified many more simple molecules like CO, CO₂, HCN, CH₄ and NH₃. But it detected also many complex organics like aliphatic carbon chains, alcohols with up to five C atoms and amines [6]. Most surprisingly it detected abundant O₂ [7]. O₂ is very reactive and was believed to have been non-existent in the protosolar nebula. Very few detections of O₂ outside the Earth have been made so far. The very good correlation with water led to the finding, that O₂ was most probably formed in the presolar stage due to radiolysis of water ice and that the water ice survived the solar system formation unchanged.

In March 2015 Rosetta performed a close flyby over the comet surface of just 15 km from the comet centre. During this flyby, dust production was high. In the mass spectra of ROSINA DFMS from this flyby an analysis of the mass spectrometry data of ROSINA DFMS revealed two mass peaks at mass 75 Da, one of which was identified as coming from the amino acid glycine. The exact mass of glycine is 75.0315 Da. There are several isomers on the exact same mass. In mass spectrometry, where ionization of the neutrals is done by electron impact, isomers can be distinguished by their fragmentation pattern as molecules are not only ionized to yield the parent ion, but also dissociate into ionized fragments according to the structure of a molecule. All of the isomers of glycine could be ruled out by looking at the specific fragmentation pattern from the electron impact ionisation in the ion source of DFMS.

Figure 1: (click on the image to view with higher resolution) a mass spectrum of mass 75 Da, taken by ROSINA/DFMS on March 28, 2015, integrated over 160 s at a distance of ~20 km from the comet.

Figure 1 shows a sample mass spectrum at 75 Da. The number of ionized particles registered on the detector is given as a function of the position on the detector which corresponds to m/z. The mass resolution of DFMS m/Δm is ~9000 at FWHM for mass 28 and decreases with increasing mass. Also on mass 75 Da we find C₃H₇O₂ (75.0441 Da) which might be a fragment of propylene glycol (C₃H₈O₂) or any of its isomers or/and of even heavier species like butanediol (C₄H₁₀O₂). Only a thorough analysis of all fragments can identify the parent of C₃H₇O₂. Details on the data analysis for ROSINA DFMS can be found in Ref.[6].

To detect glycine in the coma of 67P was quite surprising as glycine has a sublimation temperature of 140°C (8), a lot higher than the comet surface (9). Analysis of the flyby revealed that the density of glycine did not follow the expected 1/r² behaviour, which led to the conclusion that glycine sublimated from dust grains in the coma, which can become much hotter due to their small sizes of a few μm and their low albedo of a few % [10].

The way to form glycine on dust grains has been investigated by [11-13]. It can be formed from the precursor molecule methylamine which was also found in the mass spectra of DFMS together with CO₂. It is up to now the only amino acid where a path for formation is known without involving liquid water. It is therefore not surprising that a search for other amino acids like e.g. alanine was unsuccessful, as the comet most probably never had liquid water.

As glycine is probably mostly on dust grains and its sublimation temperature is high, it is not possible to determine the glycine abundance in the nucleus. The abundance in the coma varies relative to water between 0 and 0.0025. Glycine is not always detected in the spectra of DFMS. We preferentially see a signal from glycine during the perihelion passage between spring 2015 and September 2015 and only if the spacecraft was close enough to the comet.

The precursor molecules methylamine and ethylamine are seen in the mass spectra only when glycine also is detected. The three molecules seem to be closely related which is not surprising. Chemical models show that glycine could form on dust grains via three radical-addition mechanisms at temperatures from 40-120 K [11] which is compatible with temperatures in hot cores. Glycine can also be formed involving photochemistry and CO₂ [13]. In both cases methylamine is part of the process.

Another important species for living organisms is phosphorous found in adenosine triphosphate (ATP), in the backbone of DNA and RNA, and in cell membranes. The phosphorous atom with a mass of 30.9732 Da was detected by DFMS already in October 2014. However, the search for the parent (PH3, PO, PN or HCP) was unsuccessful although these species have been detected in the interstellar medium [14-17]. This is mostly due to overlaps in the mass spectra with other species, very often with abundant sulphur bearing species.

Many of the molecules found by ROSINA DFMS in the coma of comet 67P are compatible with the idea that comets delivered key molecules for prebiotic chemistry throughout the solar system and in particular to the early Earth [18] increasing drastically the concentration of life-related chemicals by impact on a closed water body. The fact that glycine was most probably formed on dust grains in the presolar stage also makes these molecules somehow universal, which means that what happened in the solar system could probably happen elsewhere in the Universe.

This article is based on our work published in 'Science Advances', 2016 [19].

References:
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[2] Alyssa K. Cobb, Ralph E. Pudritz, "Nature's Starships. I. Observed Abundances and Relative Frequencies of Amino Acids in Meteorites", Astrophysical Journal, 783, 140 (2014). Abstract.
[3] Aaron S. Burton, Jennifer C. Stern, Jamie E. Elsila, Daniel P. Glavin, Jason P. Dworkin, "Understanding prebiotic chemistry through the analysis of extraterrestrial amino acids and nucleobases in meteorites", Chemical Society Reviews, 41, 5459-5472 (2012). Abstract.
[4] Jamie E. Elsila, Daniel P. Glavin, Jason P. Dworkin, "Cometary glycine detected in samples returned by Stardust", Meteoritics & Planetary Science, 44, 9, 1323–1330 (2009). Abstract.
[5] H. Balsiger, K. Altwegg, P. Bochsler, et al., SSR, 128, 745 (2007).
[6] Léna Le Roy, Kathrin Altwegg, Hans Balsiger, Jean-Jacques Berthelier, Andre Bieler, Christelle Briois, Ursina Calmonte, Michael R. Combi, Johan De Keyser, Frederik Dhooghe, Björn Fiethe, Stephen A. Fuselier, Sébastien Gasc, Tamas I. Gombosi, Myrtha Hässig, Annette Jäckel, Martin Rubin, Chia-Yu Tzou, "Inventory of the volatiles on comet 67P/Churyumov-Gerasimenko from Rosetta/ROSINA", Astronomy & Astrophysics, 583, A1 (2015). Abstract.
[7] A. Bieler, K. Altwegg, H. Balsiger, A. Bar-Nun, J.-J. Berthelier, P. Bochsler, C. Briois, U. Calmonte, M. Combi, J. De Keyser, E. F. van Dishoeck, B. Fiethe, S. A. Fuselier, S. Gasc, T. I. Gombosi, K. C. Hansen, M. Hässig, A. Jäckel, E. Kopp, A. Korth, L. Le Roy, U. Mall, R. Maggiolo, B. Marty, O. Mousis, T. Owen, H. Rème, M. Rubin, T. Sémon, C.-Y. Tzou, J. H. Waite, C. Walsh, P. Wurz, "Abundant molecular oxygen in the coma of comet 67P/Churyumov–Gerasimenko", Nature, 526, 678-681. (2015). Abstract.
[8] D. Gross, G. Grodsky, "On the Sublimation of Amino Acids and Peptides", Journal of the American Chemical Society, 77, 1678 (1955). Abstract.
[9] F. Peter Schloerb, Stephen Keihm, Paul von Allmen, Mathieu Choukroun, Emmanuel Lellouch, Cedric Leyrat, Gerard Beaudin, Nicolas Biver, Dominique Bockelée-Morvan, Jacques Crovisier, Pierre Encrenaz, Robert Gaskell, Samuel Gulkis, Paul Hartogh, Mark Hofstadter, Wing-Huen Ip, Michael Janssen, Christopher Jarchow, Laurent Jorda, Horst Uwe Keller, Seungwon Lee, Ladislav Rezac, Holger Sierks, "MIRO observations of subsurface temperatures of the nucleus of 67P/Churyumov-Gerasimenko", Astronomy & Astrophysics, 583, A29 (2015). Abstract.
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[19] Kathrin Altwegg, Hans Balsiger, Akiva Bar-Nun, Jean-Jacques Berthelier, Andre Bieler, Peter Bochsler, Christelle Briois, Ursina Calmonte, Michael R. Combi, Hervé Cottin, Johan De Keyser, Frederik Dhooghe, Bjorn Fiethe, Stephen A. Fuselier, Sébastien Gasc, Tamas I. Gombosi, Kenneth C. Hansen, Myrtha Haessig, Annette Jäckel, Ernest Kopp, Axel Korth, Lena Le Roy, Urs Mall, Bernard Marty, Olivier Mousis, Tobias Owen, Henri Rème, Martin Rubin, Thierry Sémon, Chia-Yu Tzou, James Hunter Waite, Peter Wurz, "Prebiotic chemicals—amino acid and phosphorus—in the coma of comet 67P/Churyumov-Gerasimenko", Science Advances, 2(5), e1600285 (2016). Abstract.

Demonstration of Light Induced Conical Intersections in Diatomic Molecules

Left to right: Adi Natan, Matt Ware, Phil Bucksbaum

Authors: Adi Natan¹, Matthew R Ware^1,4, Vaibhav S. Prabhudesai², Uri Lev³, Barry D. Bruner³, Oded Heber³, Philip H Bucksbaum^1,4

Affiliation:
¹Stanford PULSE Institute, SLAC National Accelerator Laboratory, Menlo Park, CA, USA
²Department of Nuclear and Atomic Physics, Tata Institute of Fundamental Research, Mumbai, India
³Faculty of Physics, the Weizmann Institute of Science, Rehovot, Israel
⁴Departments of Physics, Applied Physics, and Photon Science, Stanford University, Stanford, CA, USA

About 200 femtoseconds after you started reading this line, the first step in actually seeing it took place. In the very first step of vision, the retinal chromophores in the rhodopsin proteins in your eyes were photo-excited and then driven through a conical intersection to form a trans isomer [1]. The conical intersection is the crucial part of the machinery that allows such ultrafast energy flow. Conical intersections (CIs) are the crossing points between two or more potential energy surfaces. These tend to repel when they approach each other, but cannot stay separated everywhere in the multidimensional geometry landscape of a molecule. CIs are ubiquitous in photo-processes in polyatomic molecules and govern key phenomena such as DNA photostability [2], but they are difficult to locate, measure and control, since their positions and features depend on specific molecular system under study. It is therefore of great interest to simulate their effects.

The case for diatomic molecules is different because naturally occurring CIs cannot exist for them: Energy levels are repelled when they approach each other, and there are not enough degrees of freedom for a true crossing. However a strong laser field applied to a diatomic molecule adds one additional degree of freedom, which gives rise to a light-induced artificial CI (LICI) that is predicted to have several features in common with the poly-atomic “wild-type” CI [3-5]. More recent theoretical studies have examined various aspects of this LICI phenomenon [6-9].

The molecular dynamics in the vicinity of a LICI can be explored in the simplest laser-illuminated molecular system, the ground state of the hydrogen molecular ion, H₂⁺ [10]. An infrared laser will induce interactions between the two lowest nuclear potential energy curves, named 1sσ_g and 2pσ_u. The interaction of strong fields with H₂⁺ can be expressed by shifting one of the potential curves by the energy of one photon. The now ”dressed” potential curve crosses at some internuclear separation R where the two states are resonantly coupled by the laser field, the analog of the curve crossings at CIs in polyatomic molecules, as seen in Fig 1(a) . We define the LICI as this crossing point, when the polarization of the laser is perpendicular to the molecular axis. For other angles, there is no crossing, and the dynamics is “adiabatic”, that is, a nuclear wavepacket will travel only on one of the dressed potential curves.

Consider for a moment what it means to have a point of crossing where the field is perpendicular to the molecular axis of a diatomic molecule: This molecule effectively “feels” zero laser field only at this specific angle, so the potential curves assume their field free R-dependence only here. The key to the dynamics induced by the LICI is the special behavior of the molecule as it rotates through this special point, from an angle on one side where it experiences the field, to an angle on the other side where the field is once again felt.

The simplest place to start is H₂⁺ in its ground rotational state, interacting with a strong laser field that couples resonantly the two electronic states. The spherical symmetry of the ground state field-free nuclear probability density, changes rapidly when a strong field is turned on. We can follow how this probability density evolves in the dressed state framework. In the dressed picture, the LICI is a local maximum in the two-dimensional (R,θ) potential energy landscape, while in other angles, the population dissociates adiabatically on the unbound part of the light induced potential curve. This causes the part of the population to accumulate around the LICI and then scatter from it, similar to waves scattering from a cone shape potential barrier. However, unlike scattering of a free particle around a barrier, the scattering described here is of bound nuclear wave packet, which scatters into a multitude of rovibrational states on the ground electronic surface, similar to the non-adiabatic dynamics around a natural CI. The scattering from the LICI leads to dissociation, but imposes a scattering time delay. The coherent addition of all the scattering trajectories creates an interference pattern at various angles and kinetic energy releases (Fig 1 (b), and Fig 1(c)). These quantum interferences are a universal signature for LICIs because they arise from the nature of coherent scattering interference near a point of degeneracy.

Figure 1: [Click on the image to view with higher resolution] (a) The dressed potential energy surfaces of H₂⁺ featuring LICIs. (b) The calculated instantaneous probability of dissociation P(θ,t)_diss from a given vibrational state (for example, v=9) during the interaction with the laser pulse reveals the interference. (c) Experimental (top) and calculated (bottom) angular distributions of H₂⁺ dissociation at kinetic energy releases that correspond to specific initial vibrations states.

We have experimentally demonstrated the effects of LICIs on strong-field photodissociation of H₂⁺ by means of quantum interferences that modify the angular distributions of the dissociating fragments [10]. The interferences depend strongly on the energy difference between the initial state and the LICI. The larger the overlap between the initial state and the LICI, the larger the effective duration of interaction and the more developed the interferences. For example, we can compare the effect among different initial states, starting from an initial state that is nearly resonant, hence has a large overlap with the LICI, such as the vibrational level v = 9 in H₂⁺, to a state that is non-resonant such as v = 7. We observe in both calculation and experiment how these initial states indeed capture the different effective duration of the interaction with the LICI (Fig 1(c)).

LICIs are particularly attractive for future quantum control experiments due to their high degree of controllability using the polarization and frequency of the laser. The interaction is not limited to just a single LICI, and allows control of the timing of its appearance as well. Understanding the dynamics induced by LICIs will facilitate understanding and applicability to systems of higher complexity. Implementing and understanding LICIs in more complex systems will open the way to novel spectroscopy techniques in physics and chemistry.

References:
[1] Dario Polli, Piero Altoè, Oliver Weingart, Katelyn M. Spillane, Cristian Manzoni, Daniele Brida, Gaia Tomasello, Giorgio Orlandi, Philipp Kukura, Richard A. Mathies, Marco Garavelli, Giulio Cerullo, "Conical intersection dynamics of the primary photoisomerization event in vision", Nature, 467, 440 (2010). Abstract.
[2] B. K. McFarland, J. P. Farrell, S. Miyabe, F. Tarantelli, A. Aguilar, N. Berrah, C. Bostedt, J. D. Bozek, P. H. Bucksbaum, J. C. Castagna, R. N. Coffee, J. P. Cryan, L. Fang, R. Feifel, K. J. Gaffney, J. M. Glownia, T. J. Martinez, M. Mucke, B. Murphy, A. Natan, T. Osipov, V. S. Petrović, S. Schorb, Th. Schultz, L. S. Spector, M. Swiggers, I. Tenney, S. Wang, J. L. White, W. White, M. Gühr, "Ultrafast X-ray Auger probing of photoexcited molecular dynamics", Nature Communications, 5, 4235 (2014). Abstract.
[3] Nimrod Moiseyev, Milan Šindelka, Lorentz S. Cederbaum, "Laser-induced conical intersections in molecular optical lattices", Journal of Physics B,  41, 221001 (2008). Full Article.
[4] Milan Šindelka, Nimrod Moiseyev, Lorentz S. Cederbaum, "Strong impact of light-induced conical intersections on the spectrum of diatomic molecules", Journal of Physics B, 44, 045603 (2011). Abstract.
[5] Nimrod Moiseyev, Milan Šindelka, "The effect of polarization on the light-induced conical intersection phenomenon", Journal of Physics B, 44, 111002 (2011). Abstract.
[6] Gábor J. Halász, Ágnes Vibók, Nimrod Moiseyev, Lorenz S. Cederbaum, "Nuclear-wave-packet quantum interference in the intense laser dissociation of the D₂⁺ molecule", Physical Review A, 88, 043413 (2013). Abstract.
[7] Gábor J Halász, Ágnes Vibók, Nimrod Moiseyev, Lorenz S Cederbaum, "Light-induced conical intersections for short and long laser pulses: Floquet and rotating wave approximations versus numerical exact results", Journal of Physics B, 45, 135101 (2012). Abstract.
[8] Gábor J. Halász, Ágnes Vibók, Milan Šindelka, Lorenz S. Cederbaum, Nimrod Moiseyev, "The effect of light-induced conical intersections on the alignment of diatomic molecules", Chemical Physics, 399, 146 (2012). Abstract.
[9] G.J. Halász, A. Vibók, L.S. Cederbaum, "Direct Signature of Light-Induced Conical Intersections in Diatomics", Journal of Physical Chemistry Letters, 6, 348 (2015). Abstract.
[10] Adi Natan, Matthew R. Ware, Vaibhav S. Prabhudesai, Uri Lev, Barry D. Bruner, Oded Heber, Philip H. Bucksbaum, "Observation of Quantum Interferences via Light-Induced Conical Intersections in Diatomic Molecules", Physical Review Letters, 116, 143004 (2016). Abstract.

Polarized Light Modulates Light-Dependent Magnetic Compass Orientation in Birds

From Left to Right: Rachel Muheim, Sissel Sjöberg, Atticus Pinzon-Rodriguez

Authors: Rachel Muheim, Sissel Sjöberg, Atticus Pinzon-Rodriguez

Affiliation: Department of Biology, Lund University, Sweden.

Magnetic compass orientation of birds depends on polarization of light

A wide range of animals, including birds, use directional information from the Earth’s magnetic field for orientation and navigation [1]. The magnetic compass of birds is light dependent and suggested to be mediated by light-induced, biochemical reactions taking place in specialized photoreceptors [2,3]. The photopigment molecules form magnetically sensitive radical-pair intermediates upon light excitation. The ratio of the spin states of the radical pairs (i.e., singlet vs. triplet state) is affected by Earth-strength magnetic fields, which thereby alters the response of the photopigments to light. In birds, such magneto-sensitive photoreceptors have been proposed to be arranged in an ordered array in the eye. Depending on their alignment to the magnetic field, they would show an increased or decreased sensitivity to light [2,3]. The animals would thereby perceive the magnetic field as a magnetic modulation pattern centered on the magnetic field lines, either superimposed on the visual field or mediated by a separate channel [4]. Cryptochromes have been proposed as putative candidate receptor molecules and found to be expressed in the retinas of birds exhibiting magnetic orientation behavior [2,5–7].

Hitherto, the majority of biophysical models on magnetic field effects on radical pairs have assumed that the light activating the magnetoreceptor molecules is non-directional and unpolarized, and that light absorption is isotropic. Yet, natural skylight enters the avian retina unidirectionally, through the cornea and the lens, and is often partially polarized. Also, the putative magnetoreceptor molecules, the cryptochromes, absorb light anisotropically, i.e., they preferentially absorb light of a specific direction and polarization. This implies that the light-dependent magnetic compass is intrinsically polarization sensitive [8,9].

Zebra Finch Bird

We developed a behavioural training assay to test putative interactions between the avian magnetic compass and polarized light. Thereby, we trained zebra finches to magnetic and/or overhead polarized light cues in a 4-arm “plus” maze to find a food reward with the help of their magnetic compass [10]. We found that overhead polarized light affected the birds’ ability to use their magnetic compass. The birds were only able to reliably find the food reward when the polarized light was aligned parallel to the magnetic field, but not when it was aligned perpendicular to the magnetic field [10]. We found this effect when using both 100% and 50% polarized light.

4-arm “plus” maze.

Our findings demonstrate that the magnetic compass of birds, and likely other animals, is polarization sensitive, which is a fundamentally new property of the light-dependent magnetic compass. Thus, the primary magnetoreceptor is photo- and polarization selective, as recently suggested by biophysical models [9]. The magnetic compass thus seems to be based on light-induced rotational order, thereby relaxing the requirement for an intrinsic rotational order of the receptor molecules (as long as rotational motion is restricted). The putative cryptochrome magnetoreceptors may therefore be distributed in any, also non-randomly oriented, cells in the avian retina [9]. Similar effects are expected to occur also in other organisms orienting with a light-dependent magnetic compass based on radical-pair reactions. Our findings thereby add a new dimension to the understanding of how not only birds, but animals in general, perceive the Earth’s magnetic field.

It remains to be shown to what degree birds in nature are affected by different alignments of polarized light and the Earth’s magnetic field. It could be a mechanism to enhance the magnetic field around sunrise and sunset, when polarized light is aligned roughly parallel to the magnetic field and when many migratory songbirds are believed to determine their departure direction and calibrate the different compasses with each other for the upcoming night’s flight. During midday, when polarized light and the magnetic field are aligned roughly perpendicular to each other, the magnetic field would be less prominent, thus would be less likely to interfere with visual tasks like foraging and predator detection [10].

References:
[1] Roswitha Wiltschko, Wolfgang Wiltschko, "Magnetic Orientation in Animals" (Springer, 1995).
[2] Thorsten Ritz, Salih Adem, Klaus Schulten, "A model for photoreceptor-based magnetoreception in birds", Biophysics Journal, 78, 707–718 (2000). Article.
[3] Christopher T. Rodgers, P. J. Hore, "Chemical magnetoreception in birds: The radical pair mechanism", Proceedings of the National Academy of Sciences, 106, 353–360 (2009). Abstract.
[4] Ilia A. Solov'yov, Henrik Mouritsen, Klaus Schulten, "Acuity of a cryptochrome and vision-based magnetoreception system in birds", Biophysics Journal, 99, 40–49 (2010). Article.
[5] Miriam Liedvoge, Henrik Mouritsen, "Cryptochromes—a potential magnetoreceptor: what do we know and what do we want to know?" Journal of Royal Society Interface, 7, S147 –S162 (2010). Abstract.
[6] Christine Nießner, Susanne Denzau, Julia Christina Gross, Leo Peichl, Hans-Joachim Bischof, Gerta Fleissner, Wolfgang Wiltschko, Roswitha Wiltschko, "Avian ultraviolet/violet cones identified as probable magnetoreceptors", PLOS ONE, 6, 0020091 (2011). Abstract.
[7] Kiminori Maeda, Alexander J. Robinson, Kevin B. Henbest, Hannah J. Hogben, Till Biskup, Margaret Ahmad, Erik Schleicher, Stefan Weber, Christiane R. Timmel, P.J. Hore, "Magnetically sensitive light-induced reactions in cryptochrome are consistent with its proposed role as a magnetoreceptor", Proceedings of the National Academy of Sciences, 109, 4774–4779 (2012). Abstract.
[8] Rachel Muheim,  "Behavioural and physiological mechanisms of polarized light sensitivity in birds", Philosophical Transactions of the Royal Society B : Biological Sciences, 366, 763 –771 (2011). Abstract.
[9] Jason C.S. Lau, Christopher T. Rodgers, P.J. Hore, "Compass magnetoreception in birds arising from photo-induced radical pairs in rotationally disordered cryptochromes", Journal of Royal Society Interface, 9, 3329–3337 (2012). Abstract.
[10] Rachel Muheima, Sissel Sjöberga, Atticus Pinzon-Rodrigueza, "Polarized light modulates light-dependent magnetic compass orientation in birds", Proceedings of the National Academy of Sciences, 113, 1654-1659 (2016). Abstract.