Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically

Yajie Zhou; Tianyang Tong; Mengke Wei; Peng Zhang; Fan Fei; Xiujuan Zhou; Zhen Guo; Jing Zhang; Huangtao Xu; Lei Zhang; Shun Wang; Junfeng Wang; Tiantian Cai; Xin Zhang; Can Xie

doi:10.24272/j.issn.2095-8137.2022.423

Volume 44 Issue 1

Jan. 2023

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Article Navigation > Zoological Research > 2023 > 44(1): 142-152

Yajie Zhou, Tianyang Tong, Mengke Wei, Peng Zhang, Fan Fei, Xiujuan Zhou, Zhen Guo, Jing Zhang, Huangtao Xu, Lei Zhang, Shun Wang, Junfeng Wang, Tiantian Cai, Xin Zhang, Can Xie. Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically. Zoological Research, 2023, 44(1): 142-152. doi: 10.24272/j.issn.2095-8137.2022.423

Citation:

Yajie Zhou, Tianyang Tong, Mengke Wei, Peng Zhang, Fan Fei, Xiujuan Zhou, Zhen Guo, Jing Zhang, Huangtao Xu, Lei Zhang, Shun Wang, Junfeng Wang, Tiantian Cai, Xin Zhang, Can Xie. Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically. Zoological Research, 2023, 44(1): 142-152. doi: 10.24272/j.issn.2095-8137.2022.423

Citation:

Yajie Zhou, Tianyang Tong, Mengke Wei, Peng Zhang, Fan Fei, Xiujuan Zhou, Zhen Guo, Jing Zhang, Huangtao Xu, Lei Zhang, Shun Wang, Junfeng Wang, Tiantian Cai, Xin Zhang, Can Xie. Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically. Zoological Research, 2023, 44(1): 142-152. doi: 10.24272/j.issn.2095-8137.2022.423

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Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically

doi: 10.24272/j.issn.2095-8137.2022.423

Yajie Zhou^{1, 2},
Tianyang Tong^{3, 2},
Mengke Wei^{1, 2},
Peng Zhang^{2, 4},
Fan Fei^{2, 4},
Xiujuan Zhou^{2, 4},
Zhen Guo⁵,
Jing Zhang^{2, 4},
Huangtao Xu²,
Lei Zhang^{2, 4},
Shun Wang^{1, 2, 4},
Junfeng Wang^{1, 2, 4, 6},
Tiantian Cai⁷,
Xin Zhang^{1, 2, 4, 6},
Can Xie^{2, 4, 6
,
,}

1.
Institutes of Physical Science and Information Technology, Anhui University, Hefei, Anhui 230039, China
2.
High Magnetic Field Laboratory, Hefei Institutes of Physical Science, Chinese Academy of Sciences, Science Island, Hefei, Anhui 230031, China
3.
Department of Anatomy, Anhui Medical University, Hefei, Anhui 230032, China
4.
Science Island Branch of Graduate School, University of Science and Technology of China, Hefei, Anhui 230036, China
5.
School of Life Sciences, Peking University, Beijing 100871, China
6.
International Magnetobiology Frontier Research Center, Science Island, Hefei, Anhui 230031, China
7.
Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, 250 Longwood Avenue, Boston, MA 02115, USA

Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
C.X. conceived the idea and designed the study. Y.Z. carried out protein purification, site-directed mutagenesis, ferrozine assay, CD spectroscopy, and EPR experiments. Y.Z. and C.X. performed data analysis. P.Z and L.Z. helped with SQUID measurement and data analysis. T.T, M.W., P.Z., F.F., X.Z., Z.G., J.Z., H.X., L.Z., and S.W. provided valuable suggestions on data analysis. Y.Z. and C.X. wrote the paper. T.C., J.W., and X.Z. provided valuable discussions and edited the manuscript. All authors read and approved the final version of the manuscript.

Funds: This study was supported by the National Natural Science Foundation of China (31640001 to C.X., U21A20148 to X.Z. and C.X.), and the Presidential Foundation of Hefei Institutes of Physical Science, Chinese Academy of Sciences (Y96XC11131, E26CCG27, and E26CCD15 to C.X.)

More Information

Corresponding author: E-mail: canxie@hmfl.ac.cn
Received Date: 2022-11-18
Accepted Date: 2022-12-07

Published Online: 2022-12-08

Publish Date: 2023-01-18

Abstract

Abstract

The ability to navigate long distances is essential for many animals to locate shelter, food, and breeding grounds. Magnetic sense has evolved in various migratory and homing species to orient them based on the geomagnetic field. A highly conserved iron-sulfur cluster assembly protein IscA is proposed as an animal magnetoreceptor (MagR). Iron-sulfur cluster binding is also suggested to play an essential role in MagR magnetism and is thus critical in animal magnetoreception. In the current study, we provide evidence for distinct iron binding and iron-sulfur cluster binding in MagR in pigeons, an avian species that relies on the geomagnetic field for navigation and homing. Pigeon MagR showed significantly higher total iron content from both iron- and iron-sulfur binding. Y65 in pigeon MagR was shown to directly mediate mononuclear iron binding, and its mutation abolished iron-binding capacity of the protein. Surprisingly, both iron binding and iron-sulfur binding demonstrated synergistic effects, and thus appear to be integral and indispensable to pigeon MagR magnetism. These results not only extend our current understanding of the origin and complexity of MagR magnetism, but also imply a possible molecular explanation for the huge diversity in animal magnetoreception.
- Animal magnetoreception,
- Iron-sulfur cluster binding,
- Iron binding,
- Magnetism,
- Magnetoreceptor (MagR)

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References(53)

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