The ocean's nitrogen is largely fixed by cyanobacteria, including Trichodesmium, which forms aggregates comprising hundreds of filaments arranged in organized architectures. Aggregates often form upon exposure to stress and have ecological and biophysical characteristics that differ from those of single filaments. Here, we report that Trichodesmium aggregates can rapidly modulate their shape, responding within minutes to changes in environmental conditions. Combining video microscopy and mathematical modeling, we discovered that this reorganization is mediated by "smart reversals" wherein gliding filaments reverse when their overlap with other filaments diminishes. By regulating smart reversals, filaments control aggregate architecture without central coordination. We propose that the modulation of gliding motility at the single-filament level is a determinant of Trichodesmium's aggregation behavior and ultimately of its biogeochemical role in the ocean.