Alonso, Béatrice

Abstract Magnetoreception is a remarkable ability found across a diverse range of organisms, including bacteria, birds, fish, insects, and mammals, enabling them to detect and harness the Earth’s geomagnetic field. Recently, the recruitment of biomineralizing ectosymbionts by euglenozoans was evidenced as an ecological strategy for microeukaryotes to acquire this sense. Here, we report a case of magnetosymbiosis involving a ciliate and four populations of endosymbiotic bacteria experiencing genome reduction. Among these bacteria, one group of sulphate-reducing Desulfovibrionales was found to biomineralize bundles of bullet-shaped magnetite crystals. The ciliate’s magnetotaxis mirrors that of free-living magnetotactic bacteria and euglenozoans, enabling efficient navigation in chemically stratified aquatic environments. However, in this case, magnetotaxis arises from an endosymbiotic interaction. Using a combination of optical-, confocal-, electron- and X-ray-based microscopy techniques, together with genomic analyses, these findings demonstrate that magnetosymbiosis can emerge in unicellular eukaryotic lineages through endosymbiotic integration, expanding our understanding of such interactions in aquatic ecosystems. More broadly, this work contributes to the ongoing debate on the origins of magnetoreception in eukaryotes.

Abstract Multicellular magnetotactic prokaryotes represent a unique group of obligately marine multicellular bacteria known for their ability to navigate along magnetic field lines thanks to ferrimagnetic nanocrystals. To date, two distinct spherical and ellipsoidal morphotypes have been described, typically ranging from 3 to 6 μm in diameter and comprising approximately 50 cells of the same species. Although widespread in highly reduced marine sediments, they are represented by solely three genera clustering into a monophyletic group within the Desulfobacterota. In this study, we report a third morphotype in reduced sediments of the Mediterranean Sea in Carry-le-Rouet, France, that is approximately 30 times more voluminous than any previously described form. Because their large size, we designated these multicellular bacteria as “giant” and explored their cell ultrastructure, ecological niche and physiology using magnetic enrichment and a combination of microscopy techniques and single-consortium genomics. Transmission electron microscopy and confocal microscopy images of several individual consortia revealed that they contain an average of 130 cells, each producing over 100 greigite magnetosomes arranged to optimize the overall magnetic moment. Phylogenomic analyses positioned giant multicellular magnetotactic prokaryotes, together with other morphotypes, in a previously undescribed genus and species within the Candidatus Magnetomoraceae family, named Magnetogigantoglobus mediterraneus. Although genetically divergent with a different ultrastructure, all multicellular magnetotactic prokaryotes seem to rely on sulfate reduction coupled to heterotrophy or autotrophy. We further discuss the significance of these findings in the context of the evolutionary history of multicellularity and magnetotaxis in prokaryotes.