Cryptochrome-dependent magnetoreception in a heteropteran insect continues even after 24 h in darkness

Netušil, Radek; Tomanová, Kateřina; Chodáková, Lenka; Chvalová, Daniela; Doležel, David; Ritz, Thorsten; Vácha, Martin

doi:10.1242/jeb.243000

Cited by 20 publications

(20 citation statements)

References 40 publications

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“…However, the Luc-CT response is potentiated by increasing the cytosolic availability of FAD, a common biological redox cofactor, confirming that redox reactions are at the core of magnetosensitivity 43 . The finding that alternative RPs can transduce physiological MF effects also suggests that other, nonphotochemical RPs, may contribute to magnetoreception, which is consistent with a growing list of examples reporting RP mediated magnetoreception in darkness 29,[44][45][46] . The synergistic interaction between Luc-CT and free FAD suggests the former facilitates formation of a complex that enables the transduction of a magnetic signal by the latter.…”

Section: Discussionsupporting

confidence: 81%

Essential elements of radical pair magnetosensitivity inDrosophila

Bradlaugh

Fedele²,

Munro

et al. 2021

Preprint

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SummaryMany animals use the Earth’s magnetic field (geoMF) for navigation1. The favored mechanism for magnetosensitivity involves a blue-light (BL) activated electron transfer reaction between flavin adenine dinucleotide (FAD) and a chain of tryptophan (Trp) residues within the photoreceptor protein, CRYPTOCHROME (CRY). The spin-state of the resultant radical pair (RP) and hence the concentration of CRY in its active state is influenced by the geoMF2. The canonical CRY-centric radical pair mechanism (RPM) does not, however, explain many physiological and behavioural observations2–8. Here, using electrophysiology and behavioural analyses, we assay magnetic field (MF) responses at single neuron and organismal level. We show that the 52 C-terminal (CT) amino acids of CRY, which are missing the FAD binding domain and the Trp chain, are sufficient to facilitate magnetoreception. We also show that increasing intracellular FAD potentiates both BL-induced and MF-dependent effects on the activity mediated by the CT. Additionally, high levels of FAD alone are sufficient to cause BL neuronal sensitivity and, remarkably, potentiation of this response in the co-presence of a MF. These unexpected results reveal the essential components of a primary magnetoreceptor in flies, providing strong evidence that non-canonical (i.e., non-CRY-dependent) RPs can elicit MF responses in cells.

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Section: Discussionsupporting

confidence: 81%

Essential elements of radical pair magnetosensitivity inDrosophila

Bradlaugh

Fedele²,

Munro

et al. 2021

Preprint

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“…A lot of evidence suggests that the superoxide radical is the most plausible radical under such circumstances 429,430,[434][435][436][437][438] . This is also consistent with animal magnetoreception in dark [439][440][441] , as it was suggested that during the backreaction, a radical pair is formed between flavin and an O 2 and that the radical pair reaction responds significantly to reorientation in the geomagnetic field 433,434,[442][443][444] . Such a radical pair could be generated without further absorption of light in the form of [FADH ...O -2 ].…”

Section: Cryptochrome-based Radical Pairssupporting

confidence: 85%

Magnetic field effects in biology from the perspective of the radical pair mechanism

Zadeh-Haghighi¹,

Simon²

2022

Preprint

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A large and growing body of research shows that weak magnetic fields can significantly influence various biological systems, including plants, animals, and humans. However, the underlying mechanisms behind these phenomena remain elusive. It is remarkable that the magnetic energies implicated in these effects are much smaller than thermal energies. Here we review these observations, of which there are now hundreds, and we suggest that a viable explanation is provided by the radical pair mechanism, which involves the quantum dynamics of the electron and nuclear spins of naturally occurring transient radical molecules. While the radical pair mechanism has been studied in detail in the context of avian magnetoreception, the studies reviewed here show that magnetosensitivity is widespread throughout biology. We review magnetic field effects on various physiological functions, organizing them based on the type of the applied magnetic fields, namely static, hypomagnetic, and oscillating magnetic fields, as well as isotope effects. We then review the radical pair mechanism as a potential unifying model for the described magnetic field effects, and we discuss plausible candidate molecules that might constitute the radical pairs. We review recent studies proposing that the quantum nature of the radical pairs provides promising explanations for xenon anesthesia, lithium effects on hyperactivity, magnetic field and lithium effects on the circadian clock, and hypomagnetic field effects on neurogenesis and microtubule assembly. We conclude by discussing future lines of investigation in this exciting new area of quantum biology related to weak magnetic field effects.

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“…The evolution of CRY might be shaped by its additional roles, including its involvement in seasonality, as was shown in the bean bug ( Ikeno, Katagiri, et al 2011 ; Ikeno, Numata, et al 2011 ) and in the linden bug Pyrrhocoris apterus ( Urbanova et al 2016 ). CRY proteins seem to participate in magnetoreception as was reported for CRY-d in the monarch butterflies ( Wan et al 2021 ) and Drosophila ( Yoshii et al 2009 ; Fedele et al 2014 ), and for CRY-m in cockroaches ( Bazalova et al 2016 ), P. apterus ( Netusil et al 2021 ), and birds ( Xu et al 2021 ).…”

Section: Introductionmentioning

confidence: 59%

Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock

Kotwica‐Rolinska

Chodáková

Smýkal

et al. 2021

Molecular Biology and Evolution

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Most organisms possess time-keeping devices called circadian clocks. At the molecular level, circadian clocks consist of transcription-translation feedback loops. Although some components of the negative transcription-translation feedback loop are conserved across the animals, important differences exist between typical models, such as mouse and the fruit fly. In Drosophila, the key components are PERIOD (PER) and TIMELESS (TIM-d) proteins, whereas the mammalian clock relies on PER and CRYPTOCHROME (CRY-m). Importantly, how the clock has maintained functionality during evolutionary transitions between different states remains elusive. Therefore, we systematically described the circadian clock gene setup in major bilaterian lineages and identified marked lineage-specific differences in their clock constitution. Then we performed a thorough functional analysis of the linden bug Pyrrhocoris apterus, an insect species comprising features characteristic of both the Drosophila and the mammalian clocks. Unexpectedly, the knockout of timeless-d, a gene essential for the clock ticking in Drosophila, did not compromise rhythmicity in P. apterus, it only accelerated its pace. Furthermore, silencing timeless-m, the ancestral timeless type ubiquitously present across animals, resulted in a mild gradual loss of rhythmicity, supporting its possible participation in the linden bug clock, which is consistent with timeless-m role suggested by research on mammalian models. The dispensability of timeless-d in P. apterus allows drawing a scenario in which the clock has remained functional at each step of transition from an ancestral state to the TIM-d-independent PER+CRY-mammalian system operating in extant vertebrates, including humans.

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Cryptochrome-dependent magnetoreception in a heteropteran insect continues even after 24 h in darkness

Cited by 20 publications

References 40 publications

Essential elements of radical pair magnetosensitivity inDrosophila

Essential elements of radical pair magnetosensitivity inDrosophila

Magnetic field effects in biology from the perspective of the radical pair mechanism

Loss of Timeless Underlies an Evolutionary Transition within the Circadian Clock

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