Towards magnetism in pigeon MagR: Iron- and iron-sulfur binding work indispensably and synergistically
Yajie Zhou, 安徽大学物质科学与信息技术学院, 安徽 合肥 230039, 中国, Tianyang Tong, Mengke Wei, Peng Zhang, Fei Fan, Xiujuan Zhou, Zhen Guo, Jing Zhang, Huangtao Xu, Lei Zhang, Shun Wang, Junfeng Wang, Tiantian Cai, Xin Zhang, Can Xie, 中国科学院合肥物质科学研究院强磁场科学中心, 安徽 合肥 230031, 中国, 安徽医科大学基础医学院, 安徽 合肥 230032, 中国, 中国科学技术大学研究生院科学岛分院, 安徽 合肥 230036, 中国, 北京大学生命科学学院, 北京 100871, 中国, 国际磁生物学前沿研究中心, 安徽 合肥 230031, 中国, 哈佛大学医学院生物化学和分子药理学系, 波士顿 02115, 美国
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.