One of the earliest events in the molecular evolution of photosynthesis is the structural and functional specialisation of Type I (ferredoxin-reducing) and Type II (quinone-reducing) reaction centres. In this opinion article we point out that the homodimeric Type I reaction centre of Heliobacteria has a calcium-binding site with striking structural similarities to the Mn4CaO5 cluster of Photosystem II. These similarities indicate that most of the structural elements required to evolve water oxidation chemistry were present in the earliest reaction centres. We suggest that the divergence of Type I and Type II reaction centres was made possible by a drastic structural shift linked to a change in redox properties that coincided with or facilitated the origin of photosynthetic water oxidation.