Magnetotactic advantage in stable sediment by long-term observations of magnetotactic bacteria in Earth's field, zero field and alternating field

Abstract

Magnetotactic bacteria (MTB) rely on magnetotaxis to effectively reach their preferred living habitats, whereas experimental investigation of magnetotactic advantage in stable sediment is currently lacking. We studied two wild type MTB (cocci and rod-shaped M. bavaricum) in sedimentary environment under exposure to geomagnetic field in the laboratory, zero field and an alternating field whose polarity was switched every 24 hours. The mean concentration of M. bavaricum dropped by ~50% during 6 months in zero field, with no clear temporal trend suggesting an extinction. Cell numbers recovered to initial values within ~1.5 months after the Earth's field was reset. Cocci displayed a larger temporal variability with no evident population changes in zero field. The alternating field experiment produced a moderate decrease of M. bavaricum concentrations and nearby extinction of cocci, confirming the active role of magnetotaxis in sediment and might point to a different magnetotactic mechanism for M. bavaricum which possibly benefited them to survive field reversals in geological periods. Our findings provide a first quantification of magnetotaxis advantage in sedimentary environment.

Fig 1. Magnetic field setups in zero field (a) and vertically alternating field (b).

The zero field condition was generated by three pairs of Helmholtz coils, in which sediment microcosm was placed in the center for guarantee of near-to-zero magnetic field during the experiment. In (b), two pairs of Helmholtz coils were used to compensate external horizontal and vertical field components and the third pair was responsible for reversing vertical field component. The switch upward and downward field every 24 hours was executed by an electronically controlled commutator. The downward field intensity was 118–121.5 μT and upward field intensity was -123- -120 μT.

Fig 2. Procedures of sampling and measurements.

(a) 6–9 sediment mini-cores were sampled around the 9 areas indicated by the black dots. (b) a mini-core, 25 mm long, was taken by a drinking plastic straw. Each mini-core was sliced every 1 mm increment and diluted with distilled water. (c) A drop of 10 μl diluted solution was made to be a hanging drop over an O-ring. (d) MTB number was directly obtained under the magnetodrome. (e) Transmission electron micrograph (TEM) image of a rod-shaped M. bavaricum cell with a few bundles of magnetosomes. (f) TEM image of two coccic cells with four bundles of magnetosomes in each cell.

Fig 3. Reformation of oxygen gradient in a disturbed sediment.

The sediment in a glass baker was stirred completely to form sediment slurry (1000 ml, left top). Let the sediment stabilize until a clear water-sediment interface was reached (e.g. at 14.5 hours) meanwhile oxygen profile was measured continuously from the beginning (0 hour) to reformation of stable oxygen gradient (21 hours). The contour indicated the oxic-anoxic interface which was generally stabilized in the following experiments.

Fig 4. Vertical distribution changes with time.

Development of M. bavaricum vertical distribution (square) and oxygen gradient (dotted line).

Fig 5. Vertical distribution changes with time.

Development of cocci vertical distribution (square) and oxygen gradient (dotted line).

Fig 6. Population changes of M. bavaricum (a) and cocci (b) in Earth’s field (red symbols), zero field (black symbols) and alternating field (blue symbols) as a function of time.

Filled symbols represented averaged population density of 6–9 profiles (25 mm long) and smaller open symbols represented population density of single profile. Horizontal dashed lines and numbers errors referred to mean concentration in zero field (black), Earth’s field (red) and alternating field (blue). Red filled triangle represents one sediment microcosm constantly in Earth’s field.

Fig 7. Vertical distributions in the three field settings.

Vertical distributions (average of each field setting) of M. bavaricum (a) and cocci (b) in Earth’s field, zero field and alternating field. The population intensity (cells/μl) in three field settings was inserted.