A Timeline of Bacterial and Archaeal Diversification in the Ocean

Microbial plankton play a central role in marine biogeochemical cycles, but the timing in which abundant lineages colonized contemporary ocean environments remains unclear. Here, we reconstructed the geological dates in which major clades of bacteria and archaea colonized the ocean using a high-resolution benchmarked phylogenetic tree that allows for simultaneous and direct comparison of the ages of multiple divergent lineages. Our findings show that the diversification of the most prevalent marine clades is the result of three main phases of colonization that coincide with major oxygenation events. The first phase took place after the initial oxygenation of the planet that occurred at the time of the Great Oxidation Event (2.4-2.2 Ga), after which several lineages that proliferate in oxygen minimum zones today first colonized marine niches. The second phase began around the time of the Neoproterozoic Oxidation Event (0.8-0.4 Ga) and included the diversification of the most abundant heterotrophic bacterial clades, consistent with the hypothesis that their diversification is linked to the emergence of large eukaryotic phytoplankton. The last phase encompasses prevalent cyanobacterial lineages and occurred after the Phanerozoic Oxidation Event (0.45-0.4 Ga), coinciding with the formation of the contemporary oligotrophic ocean. Our work clarifies the timing at which abundant lineages of bacteria and archaea colonized the ocean, links their adaptive radiations with key geological events, and demonstrates that the redox state of the ocean throughout Earth’s history has been the primary factor shaping the diversification of the most prevalent marine microbial clades.