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Nat Microbiol. 2019 Jul;4(7):1088-1095. doi: 10.1038/s41564-019-0432-7. Epub 2019 Apr 29.

Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist.

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CNRS, CEA, Aix-Marseille Université, UMR7265 Biosciences and Biotechnologies Institute of Aix-Marseille, Saint Paul lez Durance, France.
Génomique Métabolique, CEA, Genoscope, Institut François Jacob, CNRS, Université d'Évry, Université Paris-Saclay, Evry, France.
Sorbonne Université, UMR CNRS 7590, Muséum National d'Histoire Naturelle, IRD, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie, Paris, France.
Genoscope, Institut de biologie François Jacob, CEA, Université Paris-Saclay, Evry, France.
Institut de Radioprotection et de Sûreté Nucléaire, PRP-ENV/SERIS/LECO, Cadarache, Saint-Paul-lez-Durance, France.
Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, UMR 7154 CNRS, Paris, France.
Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam-Golm, Germany.
Ecologie Systématique Evolution, CNRS, Université Paris-Sud, Université Paris-Saclay, Agro Paris Tech, Orsay, France.
Lincoln Agritech Limited, Lincoln, New Zealand.
CNRS, CEA, Aix-Marseille Université, UMR7265 Biosciences and Biotechnologies Institute of Aix-Marseille, Saint Paul lez Durance, France.


Mutualistic symbioses are often a source of evolutionary innovation and drivers of biological diversification1. Widely distributed in the microbial world, particularly in anoxic settings2,3, they often rely on metabolic exchanges and syntrophy2,4. Here, we report a mutualistic symbiosis observed in marine anoxic sediments between excavate protists (Symbiontida, Euglenozoa)5 and ectosymbiotic Deltaproteobacteria biomineralizing ferrimagnetic nanoparticles. Light and electron microscopy observations as well as genomic data support a multi-layered mutualism based on collective magnetotactic motility with division of labour and interspecies hydrogen-transfer-based syntrophy6. The guided motility of the consortia along the geomagnetic field is allowed by the magnetic moment of the non-motile ectosymbiotic bacteria combined with the protist motor activity, which is a unique example of eukaryotic magnetoreception7 acquired by symbiosis. The nearly complete deltaproteobacterial genome assembled from a single consortium contains a full magnetosome gene set8, but shows signs of reduction, with the probable loss of flagellar genes. Based on the metabolic gene content, the ectosymbiotic bacteria are anaerobic sulfate-reducing chemolithoautotrophs that likely reduce sulfate with hydrogen produced by hydrogenosome-like organelles6 underlying the plasma membrane of the protist. In addition to being necessary hydrogen sinks, ectosymbionts may provide organics to the protist by diffusion and predation, as shown by magnetosome-containing digestive vacuoles. Phylogenetic analyses of 16S and 18S ribosomal RNA genes from magnetotactic consortia in marine sediments across the Northern and Southern hemispheres indicate a host-ectosymbiont specificity and co-evolution. This suggests a historical acquisition of magnetoreception by a euglenozoan ancestor from Deltaproteobacteria followed by subsequent diversification. It also supports the cosmopolitan nature of this type of symbiosis in marine anoxic sediments.

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[Available on 2020-01-01]
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