Rapid water flow triggers long-distance positive rheotaxis for thermophilic bacteria

Bacteria thrive in nearly all environments on Earth, demonstrating remarkable adaptability to physical stimuli, as well as chemicals and light. However, the mechanisms by which bacteria locate and settle in ecological niches optimal for their growth remains poorly understood. Here, we show that Thermus thermophilus, a highly thermophilic non-flagellated species of bacteria, exhibits positive rheotaxis, navigating upstream in unidirectional rapid water flow. Mimicking their natural habitat at 70°C with a water current under optical microscopy, cells traveled distances up to 1 mm in 30 min, with infrequent directional changes. This long-distance surface migration is driven by type IV pili, facilitating vertical attachment at the cell pole, and shear-induced tilting of the cell body, resulting in alignment of the leading pole toward the direction of water flow. Direct visualization of type IV pili filaments and their dynamics revealed that rheotaxis is triggered by weakened attachment at the cell pole, regulated by ATPase activity, which was further validated by mathematical modeling. Flow experiments on 15 bacterial strains and species in the Deinococcota (synonym Deinococcus Thermus) phylum revealed that positive rheotaxis is highly conserved among rod-shaped Thermaceae, but absent in spherical-shaped Deinococcus. Our findings suggest that thermophilic bacteria reach their ecological niches by responding to the physical stimulus of rapid water flow, a ubiquitous feature in hot spring environments. This study highlights unforeseen survival strategies, showcasing an evolutionary adaptation to a surface-associated lifestyle where swimming bacteria would otherwise be swept away.