Evolutionary trajectory of microbial sulfur oxidation pathways recapitulates Earth’s oxygenation history

Dissimilatory sulfur oxidation mediated by the microbial sulfur-oxidizing (Sox) multienzyme complex has played a central role in Earth's oxidative sulfur cycle. However, the evolutionary trajectory leading to its current complexity remains poorly understood. Here, we integrated expanded genomic records with geochemical evidence to reconstruct the natural history of the Sox system along a geological timeline. Our analyses traced the origin of the truncated Sox system (SoxABXYZ) prior to the Great Oxidation Event (GOE). This early form was later assembled with reverse dissimilatory sulfite reductases (rDsr), facilitating a primitive pathway for sulfate formation during the anoxic Archean eon. Following the post-GOE atmospheric oxygen rise, the truncated system incorporated SoxCD components, evolving into a more fine-tuned, oxygen-adapted pathway compared to the rDsr-coupled alternative. The subsequent spread of these Sox pathway variants was constrained by the oxygen requirements and phylogenetic backgrounds of their prokaryotic hosts, shaping the modern ecological landscape of microbial sulfur oxidation. The viral recruitment of auxiliary Sox components marked the latest evolutionary events, enabling direct manipulation of sulfur cycling over centuries-to-millennia timescales. Collectively, the reconstructed molecular timeline offers deeper insights into the evolutionary dynamics of the global oxidative sulfur cycle and its billion-year interplay with Earth's changing environments.