Abstract

Between 2.8 and 2.4 billion years ago Nature designed a method to catalytically split water into oxygen and hydrogen with sunlight, a process that humanity struggles to perform efficiently to this day. This manifested itself as the evolution from anoxygenic to oxygenic photosynthesis, a process which involved the incorporation of manganese ions from the environment by anoxygenic photosynthetic organisms, in order to utilize water as a new electron source. Recently, native bacterial reaction centers (BRCs), the protein complexes responsible for the photoelectric energy conversion of anoxygenic photosynthetic organisms, were shown to be able to utilize manganese as a secondary electron donor, an ability thought to only be possessed by oxygenic reaction centers. Here we uncovered several important details of this interaction, including the binding and donating sites of manganese in the BRCs, the rate of electron transfer from manganese to the BRC, and information on the composition of the manganese complex. This new information sheds light on the earliest step in the transition from anoxygenic to oxygenic photosynthesis, allowing an evaluation of the feasability of this potential evolutionary pathway by considering the effects of manganese on the native secondary electron donor, and on the final electron acceptor.