Conservation of magnetite biomineralization genes in all domains of life and implications for magnetic sensing

Animals use geomagnetic fields for navigational cues, yet the sensory mechanism underlying magnetic perception remains poorly understood. One idea is that geomagnetic fields are physically transduced by magnetite crystals contained inside specialized receptor cells, but evidence for intracellular, biogenic magnetite in eukaryotes is scant. Certain bacteria produce magnetite crystals inside intracellular compartments, representing the most ancient form of biomineralization known and having evolved prior to emergence of the crown group of eukaryotes, raising the question of whether magnetite biomineralization in eukaryotes and prokaryotes might share a common evolutionary history. Here, we discover that salmonid olfactory epithelium contains magnetite crystals arranged in compact clusters and determine that genes differentially expressed in magnetic olfactory cells, contrasted to nonmagnetic olfactory cells, share ancestry with an ancient prokaryote magnetite biomineralization system, consistent with exaptation for use in eukaryotic magnetoreception. We also show that 11 prokaryote biomineralization genes are universally present among a diverse set of eukaryote taxa and that nine of those genes are present within the Asgard clade of archaea Lokiarchaeota that affiliates with eukaryotes in phylogenomic analysis. Consistent with deep homology, we present an evolutionary genetics hypothesis for magnetite formation among eukaryotes to motivate convergent approaches for examining magnetite-based magnetoreception, molecular origins of matrix-associated biomineralization processes, and eukaryogenesis.

Synchrotron-Based Nano-XANES Reveals Intracellular Heterogeneity of Iron Species in Magnetotactic Bacteria

<p>This report demonstrates how scanning X-ray fluorescence microscopy (SXFM) and nanoscale X-ray absorption near-edge structure (nano-XANES) can spatially and chemically identify intracellular iron species at the single-cell level, creating an opportunity to examine the role of iron storage in magnetite biomineralization. Fe K-edge nano-XANES measurements of <i>Magnetospirillum gryphiswaldense</i> in varied iron media conditions and iron storage capacity revealed intracellular iron heterogeneities through a distinction between formed magnetosomes and intracellular iron material. This work highlights the potential of nano-XANES in providing an experimental advantage in the multidisciplinary field of biomineralization.</p>

Synchrotron-Based Nano-XANES Reveals Intracellular Heterogeneity of Iron Species in Magnetotactic Bacteria

<p>This report demonstrates how scanning X-ray fluorescence microscopy (SXFM) and nanoscale X-ray absorption near-edge structure (nano-XANES) can spatially and chemically identify intracellular iron species at the single-cell level, creating an opportunity to examine the role of iron storage in magnetite biomineralization. Fe K-edge nano-XANES measurements of <i>Magnetospirillum gryphiswaldense</i> in varied iron media conditions and iron storage capacity revealed intracellular iron heterogeneities through a distinction between formed magnetosomes and intracellular iron material. This work highlights the potential of nano-XANES in providing an experimental advantage in the multidisciplinary field of biomineralization.</p>

Iron phosphate mediated magnetite synthesis: a bioinspired approach

The biomineralization of intracellular magnetite in magnetotactic bacteria (MTB) is an area of active investigation. Previous work has provided evidence that magnetite biomineralization begins with the formation of an amorphous...

A Compass To Boost Navigation: Cell Biology of Bacterial Magnetotaxis

ABSTRACT Magnetotactic bacteria are aquatic or sediment-dwelling microorganisms able to take advantage of the Earth’s magnetic field for directed motility. The source of this amazing trait is magnetosomes, unique organelles used to synthesize single nanometer-sized crystals of magnetic iron minerals that are queued up to build an intracellular compass. Most of these microorganisms cannot be cultivated under controlled conditions, much less genetically engineered, with only few exceptions. However, two of the genetically amenable Magnetospirillum species have emerged as tractable model organisms to study magnetosome formation and magnetotaxis. Recently, much has been revealed about the process of magnetosome biogenesis and dedicated structures for magnetosome dynamics and positioning, which suggest an unexpected cellular intricacy of these organisms. In this minireview, we summarize new insights and place the molecular mechanisms of magnetosome formation in the context of the complex cell biology of Magnetospirillum spp. First, we provide an overview on magnetosome vesicle synthesis and magnetite biomineralization, followed by a discussion of the perceptions of dynamic organelle positioning and its biological implications, which highlight that magnetotactic bacteria have evolved sophisticated mechanisms to construct, incorporate, and inherit a unique navigational device. Finally, we discuss the impact of magnetotaxis on motility and its interconnection with chemotaxis, showing that magnetotactic bacteria are outstandingly adapted to lifestyle and habitat.