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The biotic and abiotic controls on major shifts in atmospheric oxygen and the persistence of low-oxygen periods over a majority of Earth’s history remain under debate. Explanations of Earth’s stepwise pattern of oxygenation have mostly neglected the effect of changing diel illumination dynamics linked to daylength, which has increased through geological time due to Earth’s rotational deceleration caused by tidal friction. Here we used microsensor measurements and dynamic modelling of interfacial solute fluxes in cyanobacterial mats to investigate the effect of changing daylength on Precambrian benthic ecosystems. Simulated increases in daylength across Earth’s historical range boosted the diel benthic oxygen export, even when the gross photosynthetic production remained constant. This fundamental relationship between net productivity and daylength emerges from the interaction of diffusive mass transfer and diel illumination dynamics, and is amplified by metabolic regulation and microbial behaviour. We found that the resultant daylength-driven surplus organic carbon burial could have shaped the increase in atmospheric oxygen that occurred during the Great and Neoproterozoic Oxidation Events. Our suggested mechanism, which links the coinciding increases in daylength and atmospheric oxygen via enhanced net productivity, reveals a possible contribution of planetary mechanics to the evolution of Earth’s biology and geochemistry.

For a large part of earth's history, cyanobacterial mats thrived in low‐oxygen conditions, yet our understanding of their ecological functioning is limited. Extant cyanobacterial mats provide windows into the putative functioning of ancient ecosystems, and they continue to mediate biogeochemical transformations and nutrient transport across the sediment–water interface in modern ecosystems. The structure and function of benthic mats are shaped by biogeochemical processes in underlying sediments. A modern cyanobacterial mat system in a submerged sinkhole of Lake Huron (LH) provides a unique opportunity to explore such sediment–mat interactions. In the Middle Island Sinkhole (MIS), seeping groundwater establishes a low‐oxygen, sulfidic environment in which a microbial mat dominated byPhormidiumandPlanktothrixthat is capable of both anoxygenic and oxygenic photosynthesis, as well as chemosynthesis, thrives. We explored the coupled microbial community composition and biogeochemical functioning of organic‐rich, sulfidic sediments underlying the surface mat. Microbial communities were diverse and vertically stratified to 12 cm sediment depth. In contrast to previous studies, which used low‐throughput or shotgun metagenomic approaches, our high‐throughput 16SrRNAgene sequencing approach revealed extensive diversity. This diversity was present within microbial groups, including putative sulfate‐reducing taxa ofDeltaproteobacteria, some of which exhibited differential abundance patterns in the mats and with depth in the underlying sediments. The biological and geochemical conditions in theMISwere distinctly different from those in typicalLHsediments of comparable depth. We found evidence for active cycling of sulfur, methane, and nutrients leading to high concentrations of sulfide, ammonium, and phosphorus in sediments underlying cyanobacterial mats. Indicators of nutrient availability were significantly related toMISmicrobial community composition, whileLHcommunities were also shaped by indicators of subsurface groundwater influence. These results show that interactions between the mats and sediments are crucial for sustaining this hot spot of biological diversity and biogeochemical cycling.