The swimming orientation of multicellular magnetotactic prokaryotes and uncultured magnetotactic cocci in magnetic fields similar to the geomagnetic field reveals differences in magnetotaxis between them

Abstract

Magnetotactic bacteria have intracellular chains of magnetic nanoparticles, conferring to their cellular body a magnetic moment that permits the alignment of their swimming trajectories to the geomagnetic field lines. That property is known as magnetotaxis and makes them suitable for the study of bacterial motion. The present paper studies the swimming trajectories of uncultured magnetotactic cocci and of the multicellular magnetotactic prokaryote ‘Candidatus Magnetoglobus multicellularis’ exposed to magnetic fields lower than 80 μT. It was assumed that the trajectories are cylindrical helixes and the axial velocity, the helix radius, the frequency and the orientation of the trajectories relative to the applied magnetic field were determined from the experimental trajectories. The results show the paramagnetic model applies well to magnetotactic cocci but not to ‘Ca. M. multicellularis’ in the low magnetic field regime analyzed. Magnetotactic cocci orient their trajectories as predicted by classical magnetotaxis but in general ‘Ca. M. multicellularis’ does not swim following the magnetic field direction, meaning that for it the inversion in the magnetic field direction represents a stimulus but the selection of the swimming direction depends on other cues or even on other mechanisms for magnetic field detection.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data availability

The datasets generated during the current study are available from the corresponding author on reasonable request.

References

  1. Abreu F, Martins JL, Silveira TS, Keim CN, Lins de Barros HGP, Gueiras-Filho F, Lins U (2007) ‘Candidatus Magnetoglobus multicellularis’, a multicellular magnetotactic prokaryote from a hypersaline environment. Int J Syst Evol Microbiol 57:1318–1322

    CAS  Article  Google Scholar 

  2. Abreu F, Silva KT, Leao P, Guedes IA, Keim CN, Farina M, Lins U (2013) Cell adhesion, multicellular morphology, and magnetosome distribution in the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis. Microsc Microanal 19:535–543

    CAS  Article  Google Scholar 

  3. Acosta-Avalos D, Azevedo LMS, Andrade TS, Lins de Barros H (2012) Magnetic configuration model for the multicellular magnetotactic prokaryote Candidatus Magnetoglobus multicellularis. Eur Biophys J 41:405–413

    Article  Google Scholar 

  4. Almeida FP, Viana NB, Lins U, Farina M, Keim CN (2013) Swimming behaviour of the multicellular magnetotactic prokaryote ‘Candidatus Magnetoglobus multicellularis’ under applied magnetic fields and ultraviolet light. Antonie Van Leeuwenhoek 103:845–857

    Article  Google Scholar 

  5. Araujo ACV, Morillo V, Cypriano J et al (2016) Combined genomic and structural analyses of a cultured magnetotactic bacterium reveals its niche adaptation to a dynamic environment. BEM Genom 17(Suppl 8):726

    Article  Google Scholar 

  6. Bennet M, McCarthy A, Fix D, Edwards MR, Repp F, Vach P, Dunlop JWC, Sitti M, Buller GS, Klumpp S, Faivre D (2014) Influence of magnetic fields on magneto-aerotaxis. PLoS ONE 9:e101150

    Article  Google Scholar 

  7. Berg HC (2003) The rotary motor of bacterial flagella. Annu Rev Biochem 72:19–54

    CAS  Article  Google Scholar 

  8. Chen YR, Zhang R, Du HJ, Pan HM, Zhang WY, Zhou K, Li JH, Xiao T, Wu LF (2015) A novel species of ellipsoidal multicellular magnetotactic prokaryotes from Lake Yuehu in China. Environ Microbiol 17:637–647

    CAS  Article  Google Scholar 

  9. Crenshaw HC (1996) A new look at locomotion in microorganisms: rotating and translating. Am Zool 36:608–618

    Article  Google Scholar 

  10. Cui Z, Kong D, Pan Y, Zhang K (2012) On the swimming motion of spheroidal magnetotactic bacteria. Fluid Dyn Res 44:055508

    Article  Google Scholar 

  11. De Melo RD, Acosta-Avalos D (2017) Light effects on the multicellular magnetotactic prokaryote ‘Candidatus Magnetoglobus multicellularis’ are cancelled by radiofrequency fields: the involvement of radical pair mechanisms. Antonie Van Leeuwenhoek 110:177–186

    Article  Google Scholar 

  12. Felfoul O, Mohammadi M, Taherkhani S et al (2016) Magneto-aerotactic bacteria deliver drug-containing nanoliposomes to tumour hypoxic regions. Nat Nanotechnol 11:941–947

    CAS  Article  Google Scholar 

  13. Frankel RB, Blakemore RP (1980) Navigational compass in magnetic bacteria. J Mag Mag Mater 15–18:1562–1564

    Article  Google Scholar 

  14. Greenberg M, Canter K, Mahler I, Tornheim A (2005) Observation of magnetoreceptive behavior in a multicellular magnetotactic prokaryote in higher than geomagnetic fields. Biophys J 88:1496–1499

    CAS  Article  Google Scholar 

  15. Kalmijn AJ (1981) Biophysics of geomagnetic field detection. IEEE Trans Magn MAG-17: 1113–1124

    Article  Google Scholar 

  16. Keim CN, Martins JL, Abreu F, Rosado AS, Lins de Barros HGP, Borojevic R, Lins U, Farina M (2004) Multicellular life cycle of magnetotactic prokaryotes. FEMS Microbiol Lett 240:203–208

    CAS  Article  Google Scholar 

  17. Keim CN, De Melo RD, Almeida FP, Lins de Barros HGP, Farina M, Acosta-Avalos D (2018) Effect of applied magnetic fields on motility and magnetotaxis in the uncultured magnetotactic multicellular prokaryote ‘Candidatus Magnetoglobus multicellularis’. Environ Microbiol Rep 10:465–474

    CAS  Article  Google Scholar 

  18. Klumpp S, Lefevre CT, Bennet M, Faivre D (2019) Swimming with magnets: from biological organisms to synthetic devices. Phys Rep 789:1–54

    Article  Google Scholar 

  19. Kong D, Lin W, Pan Y, Zhang K (2014) Swimming motion of rod-shaped magnetotactic bacteria: the effects of shape and growing magnetic moment. Front Microbiol 5:8

    Article  Google Scholar 

  20. Leão P, Gueiros-Filho FJ, Bazylinski DA, Lins U, Abreu F (2018) Association of magnetotactic multicellular prokaryotes with Pseudoalteromonas species in a natural lagoon environment. Antonie Van Leeuwenhoek 111:2213–2223

    Article  Google Scholar 

  21. Lefevre CT, Bernadac A, Yu-Zhang K, Pradel N, Wu LF (2009) Isolation and characterization of a magnetotactic bacterial culture from the Mediterranean Sea. Environ Microbiol 11:1646–1657

    CAS  Article  Google Scholar 

  22. Lefevre CT, Santini CL, Bernadac A, Zhang WJ, Li Y, Wu LF (2010) Calcium ion-mediated assembly and function of glycosylated flagellar sheath of marine magnetotactic bacterium. Mol Microbiol 78:1304–1312

    CAS  Article  Google Scholar 

  23. Lefevre CT, Bennet M, Landau L, Vach P, Pignol D, Bazylinski DA, Frankel RB, Klumpp S, Faivre D (2014) Diversity of Magneto-aerotactic behaviors and oxygen sensing mechanisms in cultured magnetotactic bacteria. Biophys J 107:527–538

    CAS  Article  Google Scholar 

  24. Lins U, Freitas F, Keim CN, Lins de Barros H, Esquivel DMS, Farina M (2003) Simple homemade apparatus for harvesting uncultured magnetotactic microorganisms. Braz J Microbiol 34:111–116

    Article  Google Scholar 

  25. Mao X, Egli R, Petersen N, Hanzlik M, Zhao X (2014) Magnetotaxis and acquisition of detrital remanent magnetization by magnetotactic bacteria in natural sediment: first experimental results and theory. Geochem Geophys Geosyst 15:255–283

    CAS  Article  Google Scholar 

  26. Nadkarni R, Barkley S, Fradin C (2013) A comparison of methods to measure the magnetic moment of magnetotactic bacteria through analysis of their trajectories in external magnetic fields. PLoS ONE 8:e82064

    Article  Google Scholar 

  27. Nogueira FS, Lins de Barros HGP (1995) Study of the motion of magnetotactic bacteria. Eur Biophys J 24:13–21

    Article  Google Scholar 

  28. Pan Y, Lin W, Li J, Wu W, Tian L, Deng C, Liu Q, Zhu R, Winklhofer M, Petersen N (2009) Reduced efficiency of magnetotaxis in magnetotactic coccoid bacteria in higher than geomagnetic fields. Biophys J 97:986–991

    CAS  Article  Google Scholar 

  29. Perantoni M, Esquivel DMS, Wajnberg E, Acosta-Avalos D, Cernicchiaro G, Lins de Barros H (2009) Magnetic properties of the microorganism Candidatus Magnetoglobus multicellularis. Naturwissenschaften 96:685–690

    CAS  Article  Google Scholar 

  30. Pinto O Jr, Gonzalez WD, Pinto IRCA, Gonzalez ALC, Mendes O Jr (1992) The South Atlantic Magnetic Anomaly: three decades of research. J Atmos Terr Phys 54:1129–1134

    Article  Google Scholar 

  31. Posfai M, Lefèvre CT, Trubitsyn D, Bazylinski DA, Frankel RB (2013) Phylogenetic significance of composition and crystal morphology of magnetosome minerals. Front Microbiol 4:344

    Article  Google Scholar 

  32. Silva KT, Abreu F, Almeida FP, Keim CN, Farina M, Lins U (2007) Flagellar apparatus of South-seeking many-celled magnetotactic prokaryotes. Microsc Res Technol 70:10–17

    Article  Google Scholar 

  33. Wiltschko R, Wiltschko W (2006) Magnetoreception. BioEssays 28:157–168

    CAS  Article  Google Scholar 

  34. Yan L, Zhang S, Chen P, Liu H, Yin H, Li H (2012) Magnetotactic bacteria, magnetosomes and their application. Microbiol Res 167:507–519

    CAS  Article  Google Scholar 

  35. Yang C, Chen C, Ma Q, Wu L, Song T (2012) Dynamic model and motion mechanism of magnetotactic bacteria with two lateral flagellar bundles. J Bionic Eng 9:200–210

    Article  Google Scholar 

  36. Zhang WY, Zhou K, Pan HM, Yue HD, Jiang M, Xiao T, Wu LF (2012) Two genera of magnetococci with bean-like morphology from intertidal sediments of the Yellow Sea, China. Appl Environ Microbiol 78:5606–5611

    CAS  Article  Google Scholar 

  37. Zhang SD, Petersen N, Zhang WJ, Cargou S, Ruan J, Murat D, Santini CL, Song T, Kato T, Notareschi P, Li Y, Namba K, Gue AM, Wu LF (2014) Swimming behaviour and magnetotaxis function of the marine bacterium strain MO-1. Environ Microbiol Rep 6:14–20

    CAS  Article  Google Scholar 

Download references

Acknowledgements

D. Acosta-Avalos acknowledges financial support from Fundação do Amparo à Pesquisa do Rio de Janeiro (FAPERJ). R. D. de Melo thanks Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq) for PIBIC grant. F. Abreu acknowledges support from FAPERJ, Conselho Nacional de Desenvolvimento Cientifico e Tecnologico (CNPq), Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and thanks to the microscopy facilities CENABIO-UFRJ and UniMicro-UFRJ.

Author information

Affiliations

Authors

Contributions

RDM executed experimental work related to the movement recording and obtained the trajectory coordinates, DAA and RDM designed experimental work, PL and FA executed the transmission electron microscopy, DAA and FA conducted data analyses and wrote the manuscript.

Corresponding author

Correspondence to Daniel Acosta-Avalos.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary Video 1: Uncultured magnetotactic cocci are initially concentrated in the drop border and depart from it when the magnetic field is inverted. From this type of video the trajectory coordinates were obtained using the software ImageJ. Not all MTB can be followed in the video, but using several videos we were able to get from 40 to 48 trajectories. (AVI 187 kb)

Supplementary Video 2: Ca. ‘Magnetoglobus multicellularis’ are initially concentrated in the drop border and depart from it when the magnetic field is inverted. From this type of video the trajectory coordinates were obtained using the software ImageJ. Using several videos we were able to get from 37 to 41 trajectories. (AVI 218 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

de Melo, R.D., Leão, P., Abreu, F. et al. The swimming orientation of multicellular magnetotactic prokaryotes and uncultured magnetotactic cocci in magnetic fields similar to the geomagnetic field reveals differences in magnetotaxis between them. Antonie van Leeuwenhoek 113, 197–209 (2020). https://doi.org/10.1007/s10482-019-01330-3

Download citation

Keywords

  • Magnetotaxis
  • Magnetotactic bacteria
  • Taxis/tactic responses
  • Bacterial swimming
  • Cylindrical helix swimming trajectory