On the origin of microbial magnetoreception

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.

Figure 1.

A magnetotactic bacterium (∼2.2 μm in length) with a single chain of Fe₃O₄ magnetosomes (brown inclusions). A flagellum is inserted schematically on the right side of the cell. Magnetosomes impart a permanent magnetic dipole moment to the cell and act as an internal compass needle, causing it to align passively along geomagnetic field lines as it swims.

Figure 2.

Proposed scenarios for the evolution of magnetotaxis in bacteria at or above the class or phylum taxonomic levels [35]. The last common ancestor of magnetotactic bacteria (MTB) was either (a) magnetite-producing or (b) a bacterium containing an unknown magnetosome type. Both scenarios suggest a monophyletic origin of magnetosome gene clusters (MGCs) from a single common ancestor that existed early in Earth history. Vertical inheritance followed by multiple independent gene losses is a major force that drove the evolution of magnetotaxis in bacteria at or above the class or phylum levels [35,36], while, within lower-level ranks, the evolutionary history of magnetotaxis appears to be much more complicated (e.g. [81–83]).

Figure 3.

Transmission electron microscope images of uncultured environmental magnetotactic bacteria with (a) three, (b) four and (c) five magnetosome particles per cell (white arrows point to each magnetosome), which indicates that three to five magnetosomes may provide a sufficient magnetic dipole moment for magnetotaxis in these bacteria.

Figure 4.

Exaptation model of microbial magnetoreception on early Earth. (a) Reactive oxygen species (ROS) were a major challenge to which ancient life had to adapt. ROS would have been generated and enhanced through ultraviolet radiation (UVR) (yellow), accumulating free Fe(II) inside cells (purple) and/or mineral-induced formation (orange). (b) The ancestral role of intracellular iron-oxide nanoparticles (initial magnetosomes) formed through ancient biomineralization processes was to help early life cope with oxidative stress because of their antioxidant enzyme-like activities and reducing intracellular free iron. (c) Initial magnetosomes were later co-opted to serve an additional new role of magnetoreception as a mineral magnetic sensor. (d) Modification of magnetosomes by natural selection, such as the increase in magnetosome particles and formation of a chain arrangement, would impart a greater magnetic dipole moment to the cell, leading to much more efficient magnetotaxis.