From flagellar motor behavior to bacterial swimming: defining a reference state for motility dynamics in Magnetospirillum gryphiswaldense

Abstract

Cell motility is powered by the bacterial flagellar motor, a rotary nanomachine whose activity is dynamically modulated by external stimuli. In Magnetospirillum gryphiswaldense, magnetic and chemical inputs are thought to converge at the level of motility control, yet the mechanisms underlying chemotactic regulation remain poorly understood. Here, we seek to establish a quantitative reference-state of a model strain of magnetotactic bacteria through bacterial flagellar motor dynamics. To achieve this goal, magnetotaxis was kept as a natural factor by keeping the earth's magnetic field as the only source of magnetism. To avoid aerotaxis bias, oxygen gradients were removed by implementing two different constant oxygen conditions: environmental oxygen exposure, and limited oxygen exposure. Together, the tethered-cell bacterial flagellar rotational assay and the free-swimming assay in the absence of external stimuli presented in this paper establish a framework for investigating motor and cellular swimming adaptation to magnetic, aerotactic, and chemical signals. Under reference-state conditions, the bacterial flagellar motor showed a tendency to exhibit log-normal distributions for the time spent in each motor state: runs in different directions (counter-clockwise and clockwise), and pause. A semi-Markov reference-state model was developed to provide a quantitative description of bacterial flagellar motor dynamics. The model revealed that cell magnetic polarity modulates the transition pathways leading to the paused state, whereas oxygen, in the absence of a gradient, primarily regulates residence in each motility state.