The “Dolomite Problem” has been a controversy for over a century, owing to massive assemblages of low-temperature dolomite in ancient rocks with little dolomite forming today despite favorable geochemical conditions. Experiments show that microbes and their exopolymeric substances (EPS) nucleate dolomite. However, factors controlling ancient abundances of dolomite can still not be explained. To decode the enigma of ancient dolomite, we examined a modern dolomite forming environment, and found that a cyclic shift in microbial community between cyanobacteria and anoxygenic phototrophs creates EPS suited to dolomite precipitation. Specifically, EPS show an increased concentration of carboxylic functional groups as microbial composition cycles from cyanobacterial to anoxygenic phototroph driven communities at low-and high- salinity, respectively. Comparing these results to other low-T forming environments suggests that large turnover of organic material under anoxic conditions is an important driver of the process. Consequently, the shift in atmospheric oxygen throughout Earth’s history may explain important aspects of “The Dolomite Problem”. Our results provide new context for the interpretation of dolomite throughout Earth’s history.