On the origin of microbial magnetoreception

Wei Lin; Joseph L Kirschvink; Greig A Paterson; Dennis A Bazylinski; Yongxin Pan

doi:10.1093/nsr/nwz065

On the origin of microbial magnetoreception

Natl Sci Rev. 2020 Feb;7(2):472-479. doi: 10.1093/nsr/nwz065. Epub 2019 May 21.

Authors

Wei Lin^{1

2

3}, Joseph L Kirschvink^{4

5}, Greig A Paterson^{1

6}, Dennis A Bazylinski⁷, Yongxin Pan^{1

2

3

8}

Affiliations

¹ Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing 100029, China.
² Institutions of Earth Science, Chinese Academy of Sciences, Beijing 100029, China.
³ France-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing 100029, China.
⁴ Division of Geological & Planetary Sciences, California Institute of Technology, Pasadena, CA 91125, USA.
⁵ Earth-Life Science Institute, Tokyo Institute of Technology, Tokyo 152-8551, Japan.
⁶ Department of Earth, Ocean and Ecological Sciences, University of Liverpool, Liverpool, L69 7ZE, UK.
⁷ School of Life Sciences, University of Nevada at Las Vegas, Las Vegas, NV 89154-4004, USA.
⁸ College of Earth and Planetary Sciences, University of Chinese Academy of Sciences, Beijing 100049, China.

Abstract

A broad range of organisms, from prokaryotes to higher animals, have the ability to sense and utilize Earth's geomagnetic field-a behavior known as magnetoreception. Although our knowledge of the physiological mechanisms of magnetoreception has increased substantially over recent decades, the origin of this behavior remains a fundamental question in evolutionary biology. Despite this, there is growing evidence that magnetic iron mineral biosynthesis by prokaryotes may represent the earliest form of biogenic magnetic sensors on Earth. Here, we integrate new data from microbiology, geology and nanotechnology, and propose that initial biomineralization of intracellular iron nanoparticles in early life evolved as a mechanism for mitigating the toxicity of reactive oxygen species (ROS), as ultraviolet radiation and free-iron-generated ROS would have been a major environmental challenge for life on early Earth. This iron-based system could have later been co-opted as a magnetic sensor for magnetoreception in microorganisms, suggesting an origin of microbial magnetoreception as the result of the evolutionary process of exaptation.

Keywords: biomineralization; exaptation; magnetoreception; magnetotactic bacteria.