Abstract
The magnetotactic yet uncultured species ‘Candidatus Magnetoglobus multicellularis’ is a spherical, multicellular ensemble of bacterial cells able to align along magnetic field lines while swimming propelled by flagella. Magnetotaxis is due to intracytoplasmic, membrane-bound magnetic crystals called magnetosomes. The net magnetic moment of magnetosomes interacts with local magnetic fields, imparting the whole microorganism a torque. Previous works investigated ‘Ca. M. multicellularis’ behavior when free swimming in water; however, they occur in sediments where bumping into solid particles must be routine. In this work, we investigate the swimming trajectories of ‘Ca. M. multicellularis’ close to solid boundaries using video microscopy. We applied magnetic fields 0.25–8.0 mT parallel to the optical axis of a light microscope, such that microorganisms were driven upwards towards a coverslip. Because their swimming trajectories approach cylindrical helixes, circular profiles would be expected. Nevertheless, at fields 0.25–1.1 mT, most trajectory projections were roughly sinusoidal, and net movements were approximately perpendicular to applied magnetic fields. Closed loops appeared in some trajectory projections at 1.1 mT, which could indicate a transition to the loopy profiles observed at magnetic fields ≥ 2.15 mT. The behavior of ‘Ca. M. multicellularis’ near natural magnetic grains showed that they were temporarily trapped by the particle’s magnetic field but could reverse the direction of movement to flee away. Our results show that interactions of ‘Ca. M. multicellularis with solid boundaries and magnetic grains are complex and possibly involve mechano-taxis.
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FAPERJ (Fundação Carlos Chagas Filho de Amparo a Pesquisa do Estado do Rio de Janeiro), as fellowships to D.M.S. and M.F., and also research grant to M.F.; CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), as fellowships to R.D.M. and M.F and a research grant to M.F.
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Conceptualization, CNK, DAA, and HLB; methodology, CNK and DAA; validation, CNK, DAA, MF, and HLB; formal analysis, CNK, RDM, and DAA; investigation, CNK, DMS and RDM; resources, CNK and MF; data curation, CNK and DAA; writing—original draft preparation, CNK; writing—review and editing, CNK, DMS, RDM, DAA, MF, and HLB; visualization, CNK and DAA; supervision, CNK; project administration, CNK. All authors have read and agreed to the published version of the manuscript.
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‘Ca. M. multicellularis’ swimming under a magnetic field 0.25 mT applied parallel to the optical axis of the microscope. The most obvious effect of the magnetic field is to maintain microorganisms roughly in focus, close to the coverslip. Observe that most movements are, in fact, perpendicular to the direction of the applied magnetic field. Note two microorganisms rotating, one clockwise and the other counterclockwise (AVI 20279 KB)
‘Ca. M. multicellularis’ swimming under a magnetic field 2.15 mT applied parallel to the optical axis of the microscope. Note some microorganisms swimming in sinusoidal profiles, where others swim in clockwise loops (AVI 20279 KB)
‘Ca. M. multicellularis’ swimming under a magnetic field 8.0 mT applied parallel to the optical axis of the microscope. Observe that most microorganisms move in clockwise loops and circles. Some microorganisms move slowly, seeming stuck to the glass (AVI 20414 KB)
A ‘Ca. M. multicellularis’ individual swimming under a magnetic field 8.0 mT applied parallel to the optical axis of the microscope, which performed four events of backward movement intercalated by forward movement. In forward movement, the microorganism swims in wide, clockwise loops. In backward movement, the microorganism stops briefly and then rotates in the opposite direction (counterclockwise) with a smaller radius, while focus is lost because it swims downwards. The corresponding trajectory is illustrated in Fig. 5 (AVI 18119 KB)
‘Ca. M. multicellularis’ swimming under the influence of the magnetic field of a natural permanently magnetic grain. Microorganisms follow the magnetic field lines, migrating towards the north magnetic pole of the particle, where they remain swimming around for a while. This video is part of a longer record from which trajectories illustrated in Fig. 6 and Online Resource 6 were obtained (AVI 22113 KB)
‘Ca. M. multicellularis’ swimming under the influence of the magnetic field of a natural permanently magnetic grain. It shows several microorganisms swimming around a natural magnetic particle, which intermittently swim backwards, most returning soon to the north pole of the grain. A few microorganisms seem to escape from the magnetic trap represented by the particle. This video is part of a longer record, from which the video in the Online Resource 5 the trajectories illustrated in Fig. 6 were recovered (AVI 24491 KB)
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Keim, C.N., da Silva, D.M., de Melo, R.D. et al. Swimming behavior of the multicellular magnetotactic prokaryote ‘Candidatus Magnetoglobus multicellularis’ near solid boundaries and natural magnetic grains. Antonie van Leeuwenhoek 114, 1899–1913 (2021). https://doi.org/10.1007/s10482-021-01649-w
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DOI: https://doi.org/10.1007/s10482-021-01649-w