CONTROLS ON OXYGEN (O2) PRODUCTION BY CYANOBACTERIAL MATS IN REDOX-STRATIFIED ENVIRONMENTS (Invited Presentation)

Cyanobacteria were the main source of oxygen (O₂) for the oxygenation of Earth’s atmosphere. However, the controls on O₂ production under low-O₂ conditions, which prevailed for much of the Precambrian, remain unclear. This mechanistic knowledge gap limits our ability to explain the patterns of oxygenation, especially the long low-O₂ stage in the Proterozoic. We studied cyanobacterial mats in the Middle Island Sinkhole (MIS) of Lake Huron, which represents an analog of Precambrian low-O₂ phototrophic habitats at the sulfide-oxygen interface. Microsensor measurements over diel light cycles showed that the mat transitioned from sulfide-driven anoxygenic photosynthesis to oxygenic photosynthesis and from a net sink to a net source of O₂ with increasing exposure time to light. This transition was controlled by external irradiance but also by the presence of large sulfur oxidizing bacteria on top of the mat, which delayed the onset of oxygenic photosynthesis for several hours and caused the mat to be a net sink of O₂, even under illumination. Downward migration of the sulfur oxidizing bacteria was governed by irradiance intensity and duration and the ratio of O₂ to sulfide in the overlying water column. Preliminary results suggest that timing of the migration may be related to the composition of intracellular sulfur granules within the sulfur-oxidizing bacteria.

Our results show how light intensity and duration exert critical yet complex controls on O₂ production, and have implications for how O₂ production varies as light changes with water depth, season, and daylength. The latter increased through the Precambrian as the moon receded from Earth; we simulated this increase in daylength with both experiments and modeling and found it boosted diel net benthic O₂ export significantly. We estimate that daylength-driven surplus O₂ export could account for a substantial part of increased O₂ during the Neoproterozoic Oxidation Event. Finally, molecular studies of the MIS mats identified both key sulfur-cycling bacteria and pathways and showed that they change with varying light through the seasons. Overall, these results highlight how physical, chemical, and biological dynamics conspire to shape O₂ production in cyanobacterial mats in unexpected ways, and may help to explain low-O₂ levels during the middle period of Earth’s history.