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Ectosymbiotic bacteria at the origin of magnetoreception in a marine protist

Nature Microbiology volume 4, pages 1088–1095 (2019)Cite this article

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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.

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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 MK131721–MK131747 and MK153697–MK153721, 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.

References

  1. Margulis, L. & Fester, R. Symbiosis as a Source of Evolutionary Innovation: Speciation and Morphogenesis (MIT Press, 1991).

  2. López-García, P., Eme, L. & Moreira, D. Symbiosis in eukaryotic evolution. J. Theor. Biol. 434, 20–33 (2017).

    Article  Google Scholar 

  3. Bernhard, J. M., Buck, K. R., Farmer, M. A. & Bowser, S. S. The Santa Barbara Basin is a symbiosis oasis. Nature 403, 77–80 (2000).

    Article  CAS  Google Scholar 

  4. Morris, B. E. L., Henneberger, R., Huber, H. & Moissl-Eichinger, C. Microbial syntrophy: interaction for the common good. FEMS Microbiol. Rev. 37, 384–406 (2013).

    Article  CAS  Google Scholar 

  5. Yubuki, N. & Leander, B. S. Diversity and evolutionary history of the symbiontida (Euglenozoa). Front. Ecol. Evol. 6, 100 (2018).

  6. Müller, M. et al. Biochemistry and evolution of anaerobic energy metabolism in eukaryotes. Microbiol. Mol. Biol. Rev. 76, 444–495 (2012).

    Article  Google Scholar 

  7. Mouritsen, H. Long-distance navigation and magnetoreception in migratory animals. Nature 558, 50–59 (2018).

    Article  CAS  Google Scholar 

  8. Uebe, R. & Schüler, D. Magnetosome biogenesis in magnetotactic bacteria. Nat. Rev. Microbiol. 14, 621–637 (2016).

    Article  CAS  Google Scholar 

  9. Walker, M. M. et al. Structure and function of the vertebrate magnetic sense. Nature 390, 371–376 (1997).

    Article  CAS  Google Scholar 

  10. Mora, C. V., Davison, M., Wild, J. M. & Walker, M. M. Magnetoreception and its trigeminal mediation in the homing pigeon. Nature 432, 508–511 (2004).

    Article  CAS  Google Scholar 

  11. Nordmann, G. C., Hochstoeger, T. & Keays, D. A. Magnetoreception—a sense without a receptor. PLoS Biol. 15, e2003234 (2017).

    Article  Google Scholar 

  12. Bazylinski, D. A. & Frankel, R. B. Magnetosome formation in prokaryotes. Nat. Rev. Microbiol. 2, 217–230 (2004).

    Article  CAS  Google Scholar 

  13. Popp, F., Armitage, J. P. & Schüler, D. Polarity of bacterial magnetotaxis is controlled by aerotaxis through a common sensory pathway. Nat. Commun. 5, 5398 (2014).

    Article  CAS  Google Scholar 

  14. Torres de Araujo, F. F., Pires, M. A., Frankel, R. B. & Bicudo, C. E. M. Magnetite and magnetotaxis in algae. Biophys. J. 50, 375–378 (1986).

    Article  CAS  Google Scholar 

  15. Simpson, A. G. B., VandenHoff, J., Bernard, C., Burton, H. R. & Patterson, D. J. The ultrastructure and systematic position of the euglenozoon Postgaardi mariagerensis, Fenchel et al. Arch. Protistenkd. 147, 213–225 (1997).

    Article  Google Scholar 

  16. Blakemore, R. P., Frankel, R. B. & Kalmijn, A. J. South-seeking magnetotactic bacteria in the Southern Hemisphere. Nature 286, 384–385 (1980).

    Article  Google Scholar 

  17. Edgcomb, V. P. et al. Identity of epibiotic bacteria on symbiontid euglenozoans in O2-depleted marine sediments: evidence for symbiont and host co-evolution. ISME J. 5, 231–243 (2011).

    Article  CAS  Google Scholar 

  18. Breglia, S. A., Yubuki, N., Hoppenrath, M. & Leander, B. S. Ultrastructure and molecular phylogenetic position of a novel euglenozoan with extrusive episymbiotic bacteria: Bihospites bacati n. gen. et sp. (Symbiontida). BMC Microbiol. 10, 145 (2010).

    Article  Google Scholar 

  19. Yubuki, N., Edgcomb, V. P., Bernhard, J. M. & Leander, B. S. Ultrastructure and molecular phylogeny of Calkinsia aureus: cellular identity of a novel clade of deep-sea euglenozoans with epibiotic bacteria. BMC Microbiol. 9, 16 (2009).

    Article  Google Scholar 

  20. Abreu, F. et al. Deciphering unusual uncultured magnetotactic multicellular prokaryotes through genomics. ISME J. 8, 1055–1068 (2014).

    Article  CAS  Google Scholar 

  21. Lefèvre, C. T. et al. A cultured greigite-producing magnetotactic bacterium in a novel group of sulfate-reducing bacteria. Science 334, 1720–1723 (2011).

    Article  Google Scholar 

  22. Pósfai, M., Lefèvre, C. T., Trubitsyn, D., Bazylinski, D. A. & Frankel, R. B. Phylogenetic significance of composition and crystal morphology of magnetosome minerals. Front. Microbiol. 4, 344 (2013).

    Article  Google Scholar 

  23. Moran, N. A., McLaughlin, H. J. & Sorek, R. The dynamics and time scale of ongoing genomic erosion in symbiotic bacteria. Science 323, 379–382 (2009).

    Article  CAS  Google Scholar 

  24. McCutcheon, J. P. & Moran, N. A. Extreme genome reduction in symbiotic bacteria. Nat. Rev. Microbiol. 10, 13–26 (2011).

    Article  Google Scholar 

  25. Leão, P. et al. North-seeking magnetotactic Gammaproteobacteria in the Southern Hemisphere. Appl. Environ. Microbiol. 82, 5595–5602 (2016).

    Article  Google Scholar 

  26. Simmons, S. L., Bazylinski, D. A. & Edwards, K. J. South-seeking magnetotactic bacteria in the Northern Hemisphere. Science 311, 371–374 (2006).

    Article  CAS  Google Scholar 

  27. Bray, D. (ed.) Cell Movements: From Molecules to Motility 2nd edn, 3–60 (Garland Science, 2001)..

  28. Leander, B. S. & Keeling, P. J. Symbiotic innovation in the oxymonad Streblomastix strix. J. Eukaryot. Microbiol. 51, 291–300 (2004).

    Article  Google Scholar 

  29. Rabus, R., Hansen, T. A. & Widdel, F. in The Prokaryotes (eds Rosenberg, E., DeLong, E. F., Lory, S., Stackebrandt, E. & Thompson, F.) 309–404 (Springer, 2013).

  30. Schauder, R., Eikmanns, B., Thauer, R. K., Widdel, F. & Fuchs, G. Acetate oxidation to CO2 in anaerobic bacteria via a novel pathway not involving reactions of the citric acid cycle. Arch. Microbiol. 145, 162–172 (1986).

    Article  CAS  Google Scholar 

  31. Hamann, E. et al. Environmental Breviatea harbour mutualistic Arcobacter epibionts. Nature 534, 254–258 (2016).

    Article  CAS  Google Scholar 

  32. Monteil, C. L. et al. Accumulation and dissolution of magnetite crystals in a magnetically responsive ciliate. Appl. Environ. Microbiol. 84, e02865-17 (2018).

    Article  CAS  Google Scholar 

  33. Schüler, D. The biomineralization of magnetosomes in Magnetospirillum gryphiswaldense. Int. Microbiol. 5, 209–214 (2002).

    Article  Google Scholar 

  34. Jogler, C. et al. Cultivation-independent characterization of ‘Candidatus Magnetobacterium bavaricum’ via ultrastructural, geochemical, ecological and metagenomic methods. Environ. Microbiol. 12, 2466–2478 (2010).

    Article  CAS  Google Scholar 

  35. Medlin, L., Elwood, H. J., Stickel, S. & Sogin, M. L. The characterization of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71, 491–499 (1988).

    Article  CAS  Google Scholar 

  36. Lane, D. J. in Nucleic Acid Techniques in Bacterial Systematics (eds Stackebrandt, E. & Goodfellow, M.) 115–175 (John Wiley & Sons, 1991).

  37. Pernthaler, J., Glockner, F. O., Schonhuber, W. & Amann, R. Fluorescence in situ hybridization (FISH) with rRNA-targeted oligonucleotide probes. Methods Microbiol. 30, 207–226 (2001).

    Article  CAS  Google Scholar 

  38. Cole, J. R. et al. The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res. 31, 442–443 (2003).

    Article  CAS  Google Scholar 

  39. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).

    Article  CAS  Google Scholar 

  40. Criscuolo, A. & Gribaldo, S. BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10, 210 (2010).

    Article  Google Scholar 

  41. Nguyen, L.-T., Schmidt, H. A., von Haeseler, A. & Minh, B. Q. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32, 268–274 (2015).

    Article  CAS  Google Scholar 

  42. Kalyaanamoorthy, S., Minh, B. Q., Wong, T. K. F., von Haeseler, A. & Jermiin, L. S. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587–589 (2017).

    Article  CAS  Google Scholar 

  43. Antipov, D., Korobeynikov, A., McLean, J. S. & Pevzner, P. A. hybridSPAdes: an algorithm for hybrid assembly of short and long reads. Bioinformatics 32, 1009–1015 (2016).

  44. Wick, R. R., Judd, L. M., Gorrie, C. L. & Holt, K. E. Unicycler: resolving bacterial genome assemblies from short and long sequencing reads. PLoS Comput. Biol. 13, e1005595 (2017).

    Article  Google Scholar 

  45. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25, 1754–1760 (2009).

    Article  CAS  Google Scholar 

  46. Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).

    Article  CAS  Google Scholar 

  47. Vallenet, D. et al. MicroScope in 2017: an expanding and evolving integrated resource for community expertise of microbial genomes. Nucleic Acids Res. 45, D517–D528 (2017).

    Article  CAS  Google Scholar 

  48. Huerta-Cepas, J. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. Mol. Biol. Evol. 34, 2115–2122 (2017).

    Article  CAS  Google Scholar 

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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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Authors and Affiliations

  1. CNRS, CEA, Aix-Marseille Université, UMR7265 Biosciences and Biotechnologies Institute of Aix-Marseille, Saint Paul lez Durance, France

    Caroline L. Monteil, Géraldine Adryanczyk, Nathalie Leonhardt, Damien Faivre, David Pignol & Christopher T. Lefevre

  2. Génomique Métabolique, CEA, Genoscope, Institut François Jacob, CNRS, Université d’Évry, Université Paris-Saclay, Evry, France

    David Vallenet, Valérie Barbe & Stéphanie Fouteau

  3. Sorbonne Université, UMR CNRS 7590, Muséum National d’Histoire Naturelle, IRD, Institut de Minéralogie, de Physique des Matériaux et de Cosmochimie, Paris, France

    Nicolas Menguy & Karim Benzerara

  4. Genoscope, Institut de biologie François Jacob, CEA, Université Paris-Saclay, Evry, France

    Corinne Cruaud

  5. Institut de Radioprotection et de Sûreté Nucléaire, PRP-ENV/SERIS/LECO, Cadarache, Saint-Paul-lez-Durance, France

    Magali Floriani

  6. Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Université Paris Diderot, UMR 7154 CNRS, Paris, France

    Eric Viollier

  7. Department of Biomaterials, Max Planck Institute of Colloids and Interfaces, Potsdam-Golm, Germany

    Damien Faivre

  8. Ecologie Systématique Evolution, CNRS, Université Paris-Sud, Université Paris-Saclay, Agro Paris Tech, Orsay, France

    Purificación López-García

  9. Lincoln Agritech Limited, Lincoln, New Zealand

    Richard J. Weld

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Contributions

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 Information

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

Reporting Summary

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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