In the following, we discuss two possible reasons for the apparent lack of observations supporting magneto-aerotaxis in sediment:
1. Oxygen requirements. Most MTB are microaerobic or anaerobic. In our experiments,
M. bavaricum and wild-type cocci concentrate in the uppermost 0-10 mm sediment
where the oxygen concentration under normal conditions is as high as 200 µmol/L
(Figure 3.4, Figure 3.5). If aquaria are exposed to pure oxygen, both M. bavaricum
and wild-type cocci move down by few mm (Kerstin Reimer, personal communica- tion), so that the minimum sediment depth at which living cells are detected appears to be correlated with the oxygen gradient. On the other hand, the maximum sedi- ment depth, which is the expected place where NS bacteria become SS, is unrelated to the oxygen gradient. Because this depth did not increase under anoxic conditions, the process by which NS cells become SS appears to be controlled by other factors.
3.5 Conclusions 53
2. Dependence on other electron acceptors. For aerotactic bacteria such as E. coli, nitrate or fumarate works as alternative electron acceptor (Taylor et al., 1999). The
same might be true forM. bavaricumand/or cocci, in which case magnetotaxis under
anoxic conditions is controlled by a different electron acceptor. However, the depth
distribution of M. bavaricum appears to be unrelated to nitrate concentrations and
the specific growth requirements of this bacterium are unknown.
3.5
Conclusions
In this study, we have conducted experiments to test the magneto-aerotaxis model in
sediment containing wild-type magnetotactic bacteria. The most characteristic nature
of this model, namely the occurrence of SS bacteria under anoxic condition, could not be observed. The depth distribution of MTB responded to transient changes in oxygen gradient, but not to the disappearance of it, in which case MTB profiles remained similar to the profiles observed under normal conditions. These observations suggests that magneto- aerotaxis of wild-type bacteria in sediment works in a different manner, and is probably controlled by several chemical parameters besides oxygen.
Chapter 4
Study of magnetotaxis advantage in
stable sediment: magnetotactic bacteria
in Earth’s field, zero field and
alternating field
AbstractIn this study, we assess magnetotactic advantage in sediment by long-period observations
of natural MTB populations of cocci and M. bavaricum in an aquarium exposed to the
following magnetic field configurations: (1) geomagnetic field in the laboratory (∼44 µT
with 71◦downward inclination), (2) zero field, and (3), a ∼100 µT vertical field whose
polarity is switched every 24 hours. Comparison of MTB populations in the geomagnetic field with those observed after long (∼6 months) exposure to a zero field provides a first, simple quantification of magnetotaxis advantage in sediment. This comparison is compli- cated by extremely large spatial and temporal variations of MTB populations, whereby the cell concentration at any given depth can vary by a factor 5 between consecutive samplings within few days, and between profiles taken at few cm distance. Nevertheless, repeated sampling during normal and zero field exposure allowed detecting a decrease of MTB con- centrations in absence of a magnetic field: this effect was clearer for M. bavaricum, whose
mean concentration was 13.1± 6.1 cells/µl before cancelling the geomagnetic field, and
5.8± 1.2 cells/µl 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 geo-
56 4. Study of magnetotaxis advantage in stable sediment
field. Cocci displayed a larger temporal variability with 11.7 ± 4.5 cells/µl during stable periods in the geomagnetic field, and 11.5±4.3 cells/µl during zero field experiments. The absence of a magnetic field does not appear to produce cocci extinction in ∼6 months, nor was a significant change in depth distribution observed. A second experiment in which the polarity of a vertical magnetic field was switched on a daily basis produced a moderate
decrease of M. bavaricum concentrations and nearby extinction of cocci.
Overall, both types of MTB benefit from the presence of a magnetic field with correct polarity (i.e. pointing downward in the northern hemisphere), and this benefit appears
stronger for M. bavaricum than for cocci. While M. bavaricum drops very rapidly after
the onset of zero field conditions, recover to normal concentrations after restoring the geomagnetic field appears gradual and might be explained by its natural duplication rate. On the other hand, cocci are intolerant to reversed magnetic fields, as expected from the polar magneto-aerotaxis model of Frankel et al. (1997), confirming the active role of
magnetotaxis in sediment, while M. bavaricum is only partially affected. The reason for
this difference is unclear and might point to a different magnetotactic mechanism for M.
bavaricum.
4.1
Introduction
In presence of external magnetic field, magnetotactic bacteria (MTB) in water environment are aligned and swim along the magnetic field lines. This behaviour–known as magneto- taxis is expected to be advantageous for searching optimal living habitat in chemically stratified sediment, which can be realized in two ways: by reducing searching path from three dimension to one dimension (Kirschvink, 1980) and/or by improving MTB sensing ability (Smith et al., 2006). Reducing searching path depends on good alignment with external field. The study of magnetotactic bacteria orientation in sediment revealed that the alignment degree along the magnetic field is as low as 1% which is however sufficient for successful magnetotaxis in sediment (see chapter 2).
The unsuccessful search polar magneto-aerotaxis in uncultured cocci (chapter 3), which appear to persist in a NS state even under anoxic conditions can in principle be explained by a complex reaction to a range of other stimuli, such as tactile ones, that cannot be reproduced under the optical microscope. On the other hand, it is also possible that magnetotaxis of our MTB populations works on fundamentally different principles. For instance, MTB swimming consistently downwards in the geomagnetic field could efficiently
4.2 Materials and methods 57
escape bioturbation-induced sediment resuspension by re-entering the sediment as fast as possible. In this case, cells would never need to reverse swimming direction, provided that it stops moving when a suitable depth in sediment is reached. Therefore, the use of magnetotaxis for maintaining MTB near the oxic-anoxic interface needs to be tested directly in sediment, because the complex combination of chemical and tactile conditions cannot be reproduced under the microscope. The simplest test that serves this purpose is the comparison of MTB abundance in the same microcosm under different magnetic field configurations. Cancelling the geomagnetic fields, in particular, eliminates magnetotaxis, because MTB no longer have a preferred swimming direction and they can solely rely on chemotaxis for displacement. A decrease in MTB abundance would therefore indicate that magnetotaxis effectively provided a biological advantage.
A different experiment is used to test two known types of magnetotaxis: axial magneto- taxis, in which the geomagnetic field just provides a reference axis for directed swimming
in both directions, as observed with the spirillum M. magnetotacticum, and polar mag-
netotaxis, in which cells subjected to given conditions (i.e. oxygen concentration above a threshold) swim only in one direction, parallel or antiparallel to the magnetic field, as observed with MC-1 cultured cocci (Frankel et al., 1997). For this purpose, the polarity of a vertical or inclined magnetic field is switched at a certain rate (e.g. once a day) so that a reference axis is provided, while the field direction (in particular its vertical component) is zero on average. Such field would still support axial magnetotaxis, but not polar mag- netotaxis, since during half of the cycles, when the field points upwards, the polarity of all cells make them swim away from the oxic-anoxic interface (Frankel et al., 1997).