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 today’s oceans.

Yet, their evolutionary history and role in shaping Earth’s 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 oxygen, increased oxidative weathering boosted marine primary productivity and POM accumulation, 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.

Diverse metabolisms share functionally and genetically similar exoenzymes. Sequence similarity network of predicted exoenzymes associated with (A) enzyme type based on sequence annotation; and (B) metabolic guild. The 1307 exoenzyme protein sequences are depicted by individual nodes (colored circles). Edges (grey lines) between the nodes indicate a pairwise BLAST e-value of 1×10-30 345 . Each exoenzyme sequence is represented by a node (colored circle); 1,267 nodes are grouped into 48 clusters (e-value of 1×10-30 346 ) based on high sequence similarity, though 40 sequences were dissimilar from all other sequences and are thus not connected to any other nodes. Featured clusters (right panels) depict how diverse metabolic guilds share functionally and genetically similar exoenzymes. — biorxiv.org

Microbial exoenzymes catalyzed the transition to an oxygenated Earth, biorxiv.org

Astrobiology, genomics, evolution,