Magnetotaxis in an anaerobic ciliate via tripartite syntrophy.

Abstract

Magnetotaxis has evolved independently numerous times in bacteria, whereby genetically controlled biomineralization of nano-crystalline magnets results in swimming along Earth's magnetic field lines. Compared to magnetotactic bacteria (MTB), evolutionary mechanisms of magnetotaxis as a trait in eukaryotes remain poorly understood. Here, we report a magnetotactic ciliate, <i>Tropidoatractus magnetotacticus</i> sp. nov., that acquires magnetotaxis via syntrophy. <i>T. magnetotacticus</i> exhibits magnetotaxis due to the magnetic moment of internal ferrimagnetic magnetite (Fe₃O₄) nanoparticles forming ellipsoidal "necklace-shaped" parallel chains. Electron microscopy revealed <i>T. magnetotacticus</i> hosts numerous internal rod-shaped bacteria containing these magnetosome chains. Consistent with this, a genomic population of MTB (Thermodesulfobacteriota) in magnetically sorted <i>T. magnetotacticus</i> cells was found that encoded and expressed a magnetosome gene cluster responsible for magnetosome Fe₃O₄ biomineralization closely related to that of the ectosymbiont "<i>Candidatus</i> Desulfarcum epimagneticum." <i>T. magnetotacticus</i> also housed a second genomic population affiliated with the endosymbiotic methanogen <i>Methanoregula</i>. Metatranscriptomes of sorted <i>T. magnetotacticus</i> cells show eukaryotic hydrogenosomal Fe-hydrogenase gene expression, and expression of genes encoding proteins in an electron transport chain indicative of H₂-producing mitochondria-related organelles. Active gene expression of energy metabolism pathways indicates a tripartite syntrophic network whereby anaerobic fermentation products from <i>T. magnetotacticus</i> are consumed by two syntrophic partners: MTB producing the magnetosome chains and hydrogenotrophic methanogens. Our findings show how magnetotaxis can emerge as a trait in eukaryotes via syntrophic cooperation.