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A magnetic protein biocompass

Abstract

The notion that animals can detect the Earth’s magnetic field was once ridiculed, but is now well established. Yet the biological nature of such magnetosensing phenomenon remains unknown. Here, we report a putative magnetic receptor (Drosophila CG8198, here named MagR) and a multimeric magnetosensing rod-like protein complex, identified by theoretical postulation and genome-wide screening, and validated with cellular, biochemical, structural and biophysical methods. The magnetosensing complex consists of the identified putative magnetoreceptor and known magnetoreception-related photoreceptor cryptochromes (Cry), has the attributes of both Cry- and iron-based systems, and exhibits spontaneous alignment in magnetic fields, including that of the Earth. Such a protein complex may form the basis of magnetoreception in animals, and may lead to applications across multiple fields.

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Figure 1: The biocompass model of animal magnetoreception and navigation.
Figure 2: Genome-wide search, experimental validation and structural characterization of the magnetoreceptor MagR.
Figure 3: Molecular modelling bridges the biocompass model and the EM structures.
Figure 4: Expression of MagR and Cry in multilayers of the pigeon retina.
Figure 5: Intrinsic magnetic polarity of the magnetosensor.

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Acknowledgements

We are grateful to our colleagues in physics, zoology, biology, structural biology and genomic research fields for providing support and constructive suggestions, as these were fundamentally valuable and allowed us to complete this study. In particular, we thank Z. Xu, S. Chen, H. Cheng, J. Chou, Y. Li and J. Ji. We are grateful to GE Healthcare (Sweden) for providing a prototype Superose 6 Increase 10/300 size-exclusion column before commercial launch to separate the Cry/MagR magnetosensor protein complex, which proved to be critical in obtaining a homogeneous sample for EM structural determination. Special thanks to Å. Danielsson, L. C. Andersson, I. Salomonsson, L. Molander and F. Sundberg for technical support on chromatography. We are deeply indebted to P. Hore from University of Oxford for his advice, encouragement and comments on the manuscript. We thank Y. Zhang and Y. Rao for providing total mRNA from Drosophilia head and for helpful discussions, E. Zhang for providing Cry cDNAs from mouse and human, and Y. Sun for technical support. We thank F. Zhuang from B. ViewSolid Biotechnology for MagR knocking-out and knocking-down experiments. We also thank Core Facilities at the College of Life Sciences, Peking University, for assistance with EM data collection, and Y. Hu and X. Li for technical support.

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Contributions

C.X. conceived the idea, developed the theoretical framework, and designed the study. P.Z., T.J., S.Q. and C.X. performed the genome-wide screening of MagR candidates. S.Q. did the experimental validation of MagR. S.Q., H. Yin, C.Y. and Y.D. carried out protein purification, EM experiments and crystallization. Z.L. and H.-W.W. did the EM structural analysis. H. Yu and S.-J.L. re-sequenced cryptochromes and MagR genes from monarch butterfly and pigeon. Y.D. and H. Yin performed mutagenesis and model validation. Junfeng H., J.F. and X.Y. conducted antibody preparation and pigeon-retina experiments. Y.H., X.D. performed magnetic measurements and data analysis. Z.Z. and X.D. provided valuable suggestions on physics and navigation systems. C.X. did molecular modelling and data analysis. C.X. and S.-J.L. wrote the paper. All authors commented on the manuscript.

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Correspondence to Can Xie.

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Qin, S., Yin, H., Yang, C. et al. A magnetic protein biocompass. Nature Mater 15, 217–226 (2016). https://doi.org/10.1038/nmat4484

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