Single-cell heterogeneity underpins diatom success in dynamic ocean environments

Diatoms are the most successful and diverse phytoplankton group in the world's oceans. Here, we surveyed, at single-cell resolution, dynamic changes in the transcriptional landscape of a clonal population of Thalassiosira pseudonana as it transitioned through the light/dark cycle and fluctuations in nitrogen (N) availability conditions that simulated the end of a seasonal bloom. By profiling >7,000 single-cell transcriptomes, we have discovered extensive heterogeneity in the transcriptional states of co-existing T. pseudonana sub-populations within a clonal population. Our findings show how functionally distinct sub-populations drive adaptation of T. pseudonana to the light/dark cycle, while redistributing C and N during N-depletion. The diatom culture adapts to N-starvation through an increase in the relative size of a pre-existing sub-population expressing N-uptake and utilization genes, which enables its rapid recovery upon N-influx. We discuss how dynamic changes in the relative composition of functionally diverse sub-populations further demonstrate how anticipatory and bet-hedging strategies likely contribute to the ecological success of diatoms in the world’s oceans, by enabling their rapid adaptation to routine, as well as stressful, and unexpected environmental fluctuations.