Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist

Abstract

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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Fig. 1: Light microscope images of south-seeking magnetic protists sampled in the Mediterranean Sea, Carry-le-Rouet, France.
Fig. 2: Electron microscopy images of the magnetic protist sampled in the Mediterranean Sea, Carry-le-Rouet.
Fig. 3: Diversity of the magnetic protists and their ectosymbionts.
Fig. 4: Schematic illustration of the magnetotactic consortium showing the magnetotactic behaviour in the Northern Hemisphere and the syntrophic interactions between partners.

Data availability

Gene sequences of 18S and 16S rRNA amplified from magnetically purified populations or sorted single holobionts have been assigned to GenBank accession numbers MK131721MK131747 and MK153697MK153721, respectively. Sequencing reads and the annotated genome of strain CR-1 were deposited to the European Nucleotide Archive database under the BioProject numbers PRJEB29359 and PRJEB30760, respectively.

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Acknowledgements

This work was supported by a project from the French National Research Agency (ANR Tremplin-ERC, ANR-16-TERC-0025-01). N.M., D.F., C.L.M., D.P. and C.T.L. acknowledge support within the framework of a DFG-ANR project (ANR-14-CE35-0018). R.J.W. and C.T.L. received support from the Dumont d’Urville Science and Technology Programme (grant no. DDU-LVL1501) and New Zealand Ministry for Business, Innovation and Employment (grant no. LVLX1703). D.F. was supported by the Max Planck Society. C.T.L. also received support from the France-Berkeley Fund. P.L.-G. received support from the European Research Council Advanced Grant ‘ProtistWorld’ (grant no. 322669). The SEM facility at IMPMC was supported by funding from Région Ile de France (grant no. SESAME 2006 I-07-593/R); the transmission electron microscopy facility at IMPMC was supported by funding from Region Ile de France (grant no. SESAME 2000 E 1435). We thank A.-L. Monteil and N. Monteil for their help in collecting samples and S. Preveral for her help in confocal observation. Support for the confocal microscope was provided by the Région Provence Alpes Côte d’Azur, Conseil General of Bouches du Rhône, French Ministry of Research, CNRS and Commissariat à l’Energie Atomique et aux Energies Alternatives.

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C.L.M. and C.T.L. designed, performed and analysed most of the experiments. D.V., V.B., S.F. and C.C. designed and performed the genome sequencing and annotation. C.T.L., N.M., K.B. and M.F. performed the electron microscope analyses. E.V. performed the oxygen measurements. G.A. contributed to the identification of microorganisms. N.L. and D.F. contributed to the single-cell sorting. R.J.W. contributed to the sampling. C.L.M. and C.T.L. supervised the project with input from D.P. C.L.M. and C.T.L. wrote the first draft of the manuscript with input from P.L.-G. All authors contributed to data interpretation and editing of the paper.

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Correspondence to Christopher T. Lefevre.

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Supplementary Notes, Supplementary References, legend for Supplementary Video, Supplementary Figures 1–9 and Supplementary Tables 1 and 3.

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Supplementary Table 2

List of proteins involved in metabolic pathways found in the draft genome of Ca. Desulfarcum epimagneticum strain CR-1.

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Supplementary Video 1.

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Monteil, C.L., Vallenet, D., Menguy, N. et al. Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist. Nat Microbiol 4, 1088–1095 (2019). https://doi.org/10.1038/s41564-019-0432-7

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