Effect of applied magnetic fields on motility and magnetotaxis in the uncultured magnetotactic multicellular prokaryote 'Candidatus Magnetoglobus multicellularis'.

Magnetotactic bacteria are found in the chemocline of aquatic environments worldwide. They produce nanoparticles of magnetic minerals arranged in chains in the cytoplasm, which enable these microorganisms to align to magnetic fields while swimming propelled by flagella. Magnetotactic bacteria are diverse phylogenetically and morphologically, including cocci, rods, vibria, spirilla and also multicellular forms, known as magnetotactic multicellular prokaryotes (MMPs). We used video-microscopy to study the motility of the uncultured MMP 'Candidatus Magnetoglobus multicellularis' under applied magnetic fields ranging from 0.9 to 32 Oersted (Oe). The bidimensional projections of the tridimensional trajectories where interpreted as plane projections of cylindrical helices and fitted as sinusoidal curves. The results showed that 'Ca. M. multicellularis' do not orient efficiently to low magnetic fields, reaching an efficiency of about 0.65 at 0.9-1.5 Oe, which are four to six times the local magnetic field. Good efficiency (0.95) is accomplished for magnetic fields ≥10 Oe. For comparison, unicellular magnetotactic microorganisms reach such efficiency at the local magnetic field. Considering that the magnetic moment of 'Ca. M. multicellularis' is sufficient for efficient alignment at the Earth's magnetic field, we suggest that misalignments are due to flagella movements, which could be driven by photo-, chemo- and/or other types of taxis.

Magnetic optimization in a multicellular magnetotactic organism.

Unicellular magnetotactic prokaryotes, which typically carry a natural remanent magnetic moment equal to the saturation magnetic moment, are the prime example of magnetically optimized organisms. We here report magnetic measurements on a multicellular magnetotactic prokaryote (MMP) consisting of 17 undifferentiated cells (mean from 148 MMPs) with chains of ferrimagnetic particles in each cell. To test if the chain polarities of each cell contribute coherently to the total magnetic moment of the MMP, we used a highly sensitive magnetization measurement technique (1 fAm(2)) that enabled us to determine the degree of magnetic optimization (DMO) of individual MMPs in vivo. We obtained DMO values consistently above 80%. Numerical modeling shows that the probability of reaching a DMO > 80% would be as low as 0.017 for 17 randomly oriented magnetic dipoles. We simulated different scenarios to test whether high DMOs are attainable by aggregation or self-organization of individual magnetic cells. None of the scenarios investigated is likely to yield consistently high DMOs in each generation of MMPs. The observed high DMO values require strong Darwinian selection and a sophisticated reproduction mechanism. We suggest a multicellular life cycle as the most plausible scenario for transmitting the high DMO from one generation to the next.