Heritable diel energy reserves enhance diatom growth

Diatoms are important drivers of marine primary production and biogeochemistry1-4. Compared to other phytoplankton groups, diatoms divide more asynchronously (i.e., divisions occur in a manner that is less aligned with the diel cycle) under non-limiting conditions, resulting in divisions occurring during both day and night5-16. However, the mechanisms and rates of asynchronous division have remained elusive. Here, using microfluidics-based time-resolved cell tracking, we measure the growth dynamics of individual cells of the diatom Thalassiosira pseudonana and show that cells growing mostly during the dark phase achieve rapid generation times (8 hours), dividing as fast as cells growing fully in light. We found that this remarkable ability of rapid growth in the dark is a consequence of the light history of both the cell and its parent cell, as light history controls the amount of photosynthetic energy the cell has stored in the form of the polysaccharide chrysolaminarin when entering the night. Furthermore, a mathematical model of this mechanism yields an up to 14% increase in the daily asynchronous population growth rate compared to growth without diel energy reserves when nutrients are non-limiting. This results in an up to 17-fold predicted increase in cell abundance over a typical 10-day diatom bloom, the maximal growth advantage of heritable chrysolaminarin during exponential phases of growth. By directly demonstrating and quantifying the benefit of chrysolaminarin under different diel conditions, this work provides a mechanistic understanding of how heritable diel energy reserves contribute to the rapid growth of diatom populations in the ocean. Beyond the specific discovery of the role of heritable energy reserves, we anticipate that our experimental approach can be broadly utilized in phytoplankton research by providing a blueprint to study phytoplankton physiology and ecology at the single-cell level, revealing novel mechanisms normally obscured in bulk growth assays.