Microbial exoenzymes catalyzed the transition to an oxygenated Earth

Microbial exoenzymes--extracellular enzymes secreted to degrade complex organic polymers-- are essential for recycling carbon and nutrients, thus sustaining primary productivity in todays oceans1. Yet, their evolutionary history and role in shaping Earths early biosphere remain entirely unexplored. Here, we trace the origins of microbial exoenzymes and reveal their previously unrecognized role in driving planetary oxygenation. Our results show that exoenzymes are more common in microorganisms utilizing high-energy metabolisms, likely reflecting the energetic costs of enzyme biosynthesis and secretion. They are especially advantageous in environments rich in particulate organic matter (POM). A refined carbon cycle model indicates that early Archean oceans offered few such habitats, as low productivity and intense UV radiation rapidly photodegraded POM. However, with a Paleoproterozoic rise of atmospheric oxygen2, increased oxidative weathering boosted marine primary productivity and POM accumulation3, creating conditions favoring exoenzyme evolution. Molecular clock analyses further indicate that alkaline phosphatase, a key phosphorus-releasing exoenzyme, had likely emerged with the permanent rise of oxygen, enabling more efficient phosphorus recycling. We propose that exoenzymes initiated a positive feedback loop: by accelerating nutrient regeneration, they fueled cyanobacterial productivity and oxygen release, which in turn favored greater exoenzyme capacity, reinforcing long-term oxygenation of the planet.