Directional Matching of Swimming Polarity Provides a Competitive Advantage During Bacterial Magneto-Aerotaxis

Abstract

BackgroundMagnetotactic bacteria (MTB) utilize magnetosomes to align passively with Earths 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, optimizing 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 direct 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. ResultsWe found that a magnetic field configuration matching the predominant swimming polarity of the population results in an up to 4-fold 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 phototactic responses integrated with aerotaxis, driving collective unidirectional migration along the oxygen gradient. ConclusionsOur results provide direct evidence that matching swimming polarity with the magnetic field confers a clear advantage in 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.