Abstract
The origin and evolution of magnetoreception, which in diverse prokaryotes and protozoa is known as magnetotaxis and enables these microorganisms to detect Earth’s magnetic field for orientation and navigation, is not well understood in evolutionary biology. The only known prokaryotes capable of sensing the geomagnetic field are magnetotactic bacteria (MTB), motile microorganisms that biomineralize intracellular, membrane-bounded magnetic single-domain crystals of either magnetite (Fe3O4) or greigite (Fe3S4) called magnetosomes. Magnetosomes are responsible for magnetotaxis in MTB. Here we report the first large-scale metagenomic survey of MTB from both northern and southern hemispheres combined with 28 genomes from uncultivated MTB. These genomes expand greatly the coverage of MTB in the Proteobacteria, Nitrospirae, and Omnitrophica phyla, and provide the first genomic evidence of MTB belonging to the Zetaproteobacteria and “Candidatus Lambdaproteobacteria” classes. The gene content and organization of magnetosome gene clusters, which are physically grouped genes that encode proteins for magnetosome biosynthesis and organization, are more conserved within phylogenetically similar groups than between different taxonomic lineages. Moreover, the phylogenies of core magnetosome proteins form monophyletic clades. Together, these results suggest a common ancient origin of iron-based (Fe3O4 and Fe3S4) magnetotaxis in the domain Bacteria that underwent lineage-specific evolution, shedding new light on the origin and evolution of biomineralization and magnetotaxis, and expanding significantly the phylogenomic representation of MTB.
Highlights
Earth’s global magnetic field provides a pervasive and valuable reference frame that diverse organisms use for both short- and long-distance navigation and migration
This conclusion was made prior to the identification of conserved magnetosome gene clusters (MGCs) responsible for magnetosome biomineralization and magnetotaxis in both Fe3O4and Fe3S4-producing magnetotactic bacteria (MTB), which suggests that magnetotaxis in bacteria originated only once, so that it has a monophyletic origin [7,8,9,10,11,12]
The genomic tree was rooted with genomes from the domain Archaea
Summary
Earth’s global magnetic field provides a pervasive and valuable reference frame that diverse organisms use for both short- and long-distance navigation and migration. Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with. It has previously been suggested that magnetotaxis, based on the biomineralization of Fe3O4 and Fe3S4 in magnetosomes, in different bacterial lineages evolved independently and that MTB originated polyphyletically [6]. Recent phylogenetic analyses suggest an ancient origin of bacterial magnetotaxis in the Archean Eon, thereby making this behavior a primal physiological process and possibly one of the first examples of biomineralization on early Earth [13]. Comparison and analyses of these reconstructed genomes provide great insight into the phylogenetic diversity of MTB and the origin and evolution of magnetotaxis as well as in iron-based biomineralization on Earth. Metagenomic DNA was extracted and amplified from magnetically enriched MTB cells as previously described [13]. The average amino-acid identity (AAI) was calculated using enveomics [32]
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