Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist

• Published in: Nature microbiology Vol. 4; no. 7; pp. 1088 - 1095
• Main Authors: Monteil, Caroline L., Vallenet, David, Menguy, Nicolas, Benzerara, Karim, Barbe, Valérie, Fouteau, Stéphanie, Cruaud, Corinne, Floriani, Magali, Viollier, Eric, Adryanczyk, Géraldine, Leonhardt, Nathalie, Faivre, Damien, Pignol, David, López-García, Purificación, Weld, Richard J., Lefevre, Christopher T.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01-07-2019; Nature Publishing Group
• Subjects: 14; 14/19; 14/28; 14/32; 14/63; 45/23; 45/43; 631/181/2481; 631/326/2565/547; 631/326/41/2535; Anaerobiosis; Bacteria; Biological Coevolution; Biomedical and Life Sciences; Consortia; Deltaproteobacteria - classification; Deltaproteobacteria - genetics; Deltaproteobacteria - metabolism; Deltaproteobacteria - physiology; Division of labor; Electron microscopy; Euglenozoa - classification; Euglenozoa - microbiology; Euglenozoa - physiology; Euglenozoa - ultrastructure; Eukaryota; Ferrosoferric Oxide - metabolism; Flagella; Genes; Genome, Bacterial - genetics; Genomes; Geologic Sediments - chemistry; Geologic Sediments - microbiology; Hydrogen; Hydrogen - metabolism; Infectious Diseases; Letter; Life Sciences; Locomotion - physiology; Magnetic Fields; Magnetosomes - genetics; Magnetosomes - ultrastructure; Medical Microbiology; Metabolism; Microbiology; Motility; Motor activity; Mutualism; Nanoparticles; Oceans and Seas; Parasitology; Phylogeny; Predation; RNA, Ribosomal - genetics; rRNA 16S; rRNA 18S; Sediments; Species Specificity; Sulfate reduction; Symbiosis; Vacuoles; Virology
• ISSN: 2058-5276; 2058-5276
• DOI: 10.1038/s41564-019-0432-7

Mutualistic symbioses are often a source of evolutionary innovation and drivers of biological diversification
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. Widely distributed in the microbial world, particularly in anoxic settings
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,
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, they often rely on metabolic exchanges and syntrophy
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,
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. Here, we report a mutualistic symbiosis observed in marine anoxic sediments between excavate protists (Symbiontida, Euglenozoa)
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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 syntrophy
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. 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 magnetoreception
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acquired by symbiosis. The nearly complete deltaproteobacterial genome assembled from a single consortium contains a full magnetosome gene set
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, 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 organelles
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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.
Here, the authors identify a mutualistic symbiosis between a non-motile, magnetic deltaproteobacterium and a protist, resulting in eukaryotic magnetoreception in marine anoxic sediments.