Genomic expansion of magnetotactic bacteria reveals an early common origin of magnetotaxis with lineage-specific evolution

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.

Magnetosome magnetite biomineralization in a flagellated protist: evidence for an early evolutionary origin for magnetoreception in eukaryotes

“…Results presented here strongly indicate an early origin of magnetoreception in the domain Eukarya , a development probably evolving from a protistan ancestor that was able to synthesize magnetic nanoparticles similar to those of MTB from deeply branching phylogenetic groups. Currently, the evolution of magnetotaxis and magnetosome biomineralization in MTB is explained based on vertical and horizontal gene transfer, as well as by gene loss and gene duplication events (Lin et al ., ). Studies of magnetotactic protists would likely provide significant additional information in the evolution of magnetoreception in organisms that respond in some way to the Earth's magnetic field.…”

“…Representatives of this group are present in a number of phyla including several classes of the Proteobacteria (Sakaguchi et al ., ; Lefèvre et al ., ; Morillo et al ., ; Taoka et al ., ; Abreu et al ., ), the Nitrospirae (Lefèvre et al ., ; Lin et al ., ) and the candidate phylum Omnitrophica (Kolinko et al ., , ). Culture‐independent methods and single‐cell genome analysis indicate that the diversity and phylogenetic distribution of magnetotactic organisms are underestimated (Kolinko et al ., ; Rinke et al ., ) and may extend to other phylogenetic groups including the phyla Latescibacteria and Planctomycetes (Lin and Pan, ; Lin et al ., ; Lin et al ., ) or maybe even other domains of life (Torres de Araujo et al ., ).…”

Genomic study of a novel magnetotacticAlphaproteobacteriauncovers the multiple ancestry of magnetotaxis

“…Biomineralization of magnetic iron oxide and iron sulfide crystals by bacteria is a fascinating function whose underlying genetic determinism, molecular machinery, ecologic role and evolution have been the focus of an increasing number of investigations lately (Lefèvre et al, 2011;Lefèvre and Bazylinski, 2013;Hershey et al, 2016;Toro-Nahuelpan et al, 2016;Uebe and Schüler, 2016;Lin et al, 2017bLin et al, , 2018. To date, this ability has been observed in Gram-negative magnetotactic bacteria (MTB) only, which are commonly found at the oxic-anoxic interface (OAI) of any stratified freshwater or marine environment with an O 2 /redox gradient (Bazylinski and Frankel, 2004).…”

“…Previous biodiversity studies revealed the intriguing polyphyletism of magnetic biomineralization within the bacteria domain (Lin et al, 2018). Most of the MTB described so far belong to three classes of Proteobacteria, and some are affiliated to the Nitrospirae and Omnitrophica phyla Lin et al, 2017a).…”

Identification of novel species of marine magnetotactic bacteria affiliated with Nitrospirae phylum

“…MTB present various morphotypes including cocci, spirilla, rod-shaped, vibrio, and more complex multicellular aggregates and have been found in aquatic environments from freshwater to marine ecosystems (Blakemore, 1975;Bazylinski and Frankel, 2004;Lefevre and Bazylinski, 2013). Phylogenetically, magnetotactic bacteria are members of several classes of the Proteobacteria phylum including the Alpha-, Gamma-, Delta-, Zeta-, candidate Lambda-, candidate Eta-classes, the Nitrospirae phylum, the candidate Omnitrophica phylum, the candidate Latescibacteria phylum and the Planctomycetes phylum (Lin et al, 2017a;Lin et al, 2018).…”