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ABSTRACT The evolution of oxygenic photosynthesis in the Cyanobacteria was one of the most transformative events in Earth history, eventually leading to the oxygenation of Earth’s atmosphere. However, it is difficult to understand how the earliest Cyanobacteria functioned or evolved on early Earth in part because we do not understand their ecology, including the environments in which they lived. Here, we use a cutting-edge bioinformatics tool to survey nearly 500,000 metagenomes for relatives of the taxa that likely bookended the evolution of oxygenic photosynthesis to identify the modern environments in which these organisms live. Ancestral state reconstruction suggests that the common ancestors of these organisms lived in terrestrial (soil and/or freshwater) environments. This restricted distribution may have increased the lag between the evolution of oxygenic photosynthesis and the oxygenation of Earth’s atmosphere.IMPORTANCECyanobacteria generate oxygen as part of their metabolism and are responsible for the rise of oxygen in Earth’s atmosphere over two billion years ago. However, we do not know how long this process may have taken. To help constrain how long this process would have taken, it is necessary to understand where the earliest Cyanobacteria may have lived. Here, we use a cutting-edge bioinformatics tool called branch water to examine the environments where modern Cyanobacteria and their relatives live to constrain those inhabited by the earliest Cyanobacteria. We find that these species likely lived in non-marine environments. This indicates that the rise of oxygen may have taken longer than previously believed. 

ABSTRACT The evolution of oxygenic photosynthesis in Cyanobacteria was a transformative event in Earth's history. However, the scientific community disagrees over the duration of the delay between the origin of oxygenic photosynthesis and oxygenation of Earth's atmosphere, with estimates ranging from less than a hundred thousand to more than a billion years, depending on assumptions about rates of oxygen production and fluxes of reductants. Here, we propose a novel ecological hypothesis that a geologically significant delay could have been caused by biomolecular inefficiencies within proto‐Cyanobacteria—ancestors of modern Cyanobacteria—that limited their maximum rates of oxygen production. Consideration of evolutionary processes and genomic data suggest to us that proto‐cyanobacterial primary productivity was initially limited by photosystem instability, oxidative damage, and photoinhibition rather than nutrients or ecological competition. We propose that during the Archean era, cyanobacterial photosystems experienced protracted evolution, with biomolecular inefficiencies initially limiting primary productivity and oxygen production. Natural selection led to increases in efficiency and thus primary productivity through time. Eventually, evolutionary advances produced sufficient biomolecular efficiency that environmental factors, such as nutrient availability, limited primary productivity and shifted controls on oxygen production from physiological to environmental limitations. If correct, our novel hypothesis predicts a geologically significant interval of time between the first local oxygen production and sufficient production for oxygenation of environments. It also predicts that evolutionary rates were likely highly variable due to strong environmental selection pressures and potentially high mutation rates but low competitive interactions.