An update on polar magnetotaxis: Insights from hanging drop assays and microcosm experiments

Abstract Magnetotactic bacteria (MTB) combine passive alignment with the Earth magnetic field with a chemotactic response (magneto-chemotaxis) to reach their optimal living depth in chemically stratified environments. Current magneto-aerotaxis models fail to explain the occurrence of MTB far below the oxic-anoxic interface and the coexistence of MTB cells with opposite magnetotactic polarity at depths that are unrelated with the redox gradient. Here we propose a modified model of polar magnetotaxis which explains these observations, as well as the distinct concentration profiles and magnetotactic advantages of two types of MTB inhabiting a freshwater sediment: Magnetobacterium bavaricum (MB) and a group unidentified, wild-type cocci (MC). This model assumed that magnetotactic polarity is set by a threshold mechanism in counter gradients of oxygen and a second group of repellents, with, in case of MB, includes H⁺ ions. Depending on the position of the two repellent thresholds in a vertical redox gradient, MTB possessing this type of polar magnetotaxis either accumulate around a preferred depth where the opposed stimuli set by the two repellents are equivalent, or shuttle between two limit depths across the redox gradient (redox taxis). We show that MB belongs to the latter category, as previously postulated for MB and other members of the Nitrospirae group. Microcosm experiments suggest that redox taxis might be assisted by a partial control of magnetotactic polarity by cell metabolism, which helps maintaining a consistent polarity bias during shuttling. Our model of polar magnetotaxis supports a large variety of magnetotactic behaviors, depending on the position of the two repellent thresholds in a redox gradient, enabling different types of MTB to occupy different ecological niches in the same environment.