Coordinated motility of cyanobacteria favor mat formation, photosynthesis and carbon burial in low-oxygen, high-sulfur shallow sinkholes of Lake Huron; whereas deep-water aphotic sinkholes are analogs of deep-sea seep and vent ecosystems

Microbial life in submerged sinkhole ecosystems of the Laurentian Great Lakes is relatively understudied in comparison to seeps and vents of the deep-sea. We studied the filamentous benthic mat-forming cyanobacteria consisting primarily of Oscillatoria-like cells growing under low-light, low-oxygen and high-sulfur conditions in Lake Huron’s submerged sinkholes using in situ observations, in vitro measurements and time-lapse microscopy. Gliding movement of the cyanobacterial trichomes revealed individual as well as group-coordinated motility. When placed in a petri dish and dispersed in ground water from the sinkhole, filaments re-aggregated into defined colonies within minutes. Measured speed of individual filaments ranged from ~50 µm minute^-1 or ~15 body lengths minute^-1 to ~215 µm minute^-1 or ~70 body lengths minute^-1 – rates that are rapid relative to non-flagellated/ciliated microbes. Filaments exhibited precise and coordinated positive phototaxis towards pinpoints of light and congregated under the light of foil cutouts. Such light-responsive clusters showed an increase in photosynthetic yield – suggesting phototactic motility aids in light acquisition as well as photosynthesis. Pebbles and pieces of broken shells placed upon the mat in intact sediemnt cores were quickly covered by vertically motile filaments within hours and became fully buried in the anoxic sediments over 3-4 diurnal cycles – likely facilitating the preservation of falling plankton debris. Coordinated horizontal and vertical filament motility optimize mat cohesion and dynamics, photosynthetic efficiency and sedimentary carbon burial in modern-day sinkhole habitats where life operates across sharp redox gradients. Analogous cyanobacterial motility in the shallow seas during Earth’s early history, may have played a key role in the oxygenation of the planet by optimizing photosynthesis while favoring carbon burial. We are now eagerly mapping and exploring life in deep-water aphotic sinkholes of Lake Huron that resemble deep-sea seep and vent communities.