Directional matching of swimming polarity provides a competitive advantage during bacterial magneto-aerotaxis

BACKGROUND: Magnetotactic bacteria (MTB) utilize magnetosomes to align passively with Earth's magnetic field. Magnetic alignment, coupled with flagellar motility and aerotaxis, enables MTB to perform magneto-aerotaxis-a strategy that constrains their movement to a one-dimensional trajectory along geomagnetic field lines, which is believed to optimize their search for low-oxygen niches in aquatic environments. Beyond axially constrained movement, environmental MTB isolates exhibit a hemispherically determined swimming polarity-favoring either magnetic north or south-that has been suggested to facilitate descent into oxygen-depleted zones. However, a systematic and quantitative evaluation of how matching swimming polarity influences navigation toward low-oxygen environments has remained elusive. Here, we employed microcapillary assays to assess the functional significance of polar magneto-aerotaxis in the model organism Magnetospirillum gryphiswaldense. RESULTS: We found that a magnetic field configuration matching the predominant swimming polarity of the population results in an up to fourfold increased peak intensity of the aerotactic band compared to populations with non-matching polarity. Competition assays using fluorescently labeled north- and south-seeking populations confirmed that congruence between swimming polarity and magnetic field orientation markedly improves aerotactic band formation in oxygen gradients. Alongside our main findings, we noted biomagnetism-independent light-induced behavioral responses integrated with aerotaxis, driving collective unidirectional migration along the oxygen gradient. CONCLUSIONS: Our results provide quantitative evidence that matching swimming polarity with the magnetic field confers a clear competitive advantage over cells with an incorrect polarity when navigating oxygen gradients. These findings reinforce the role of the geomagnetic field in shaping MTB behavior and highlight the adaptive value of magnetotactic swimming polarity in environmental navigation. Our observation of light‑triggered behavior further suggests the presence of an additional sensing modality complementing magneto‑aerotactic behavior, highlighting the sophisticated sensory capabilities of M. gryphiswaldense.