Correlated responses to selection for different cell size in Chlamydomonas reinhardtii using divergent evolutionary pathways

Cell size is an important trait that is often correlated with organisms’ survival under different thermal environments, and in the case of phytoplankton, it is also related to survival under different light irradiance. While smaller phytoplankton thrive under warm and high light (summer conditions), larger cells seem to be more efficient under cool and low light conditions (winter conditions). In this study, we used different evolutionary pathways, nitrogen depletion and size selection, to select for differences in average cell diameter in the single-celled alga Chlamydomonas reinhardtii. We tested whether there was a size-related fitness (growth rate) advantage across two light intensities and two temperatures; environmental effects that have dramatic effects on algal growth. Under these environmental conditions we then tested how the evolutionary pathway to reduced cell size affected fitness and photophysiology. The results suggest that the relationship between size and growth rate in C. reinhardtii is strongly correlated with changes in the photosynthetic apparatus in different sized cells. Large-selected cells evolved to have smaller light-harvesting antennae, making them less susceptible to photodamage. However, they accumulate larger amounts of reactive oxygen species, potentially due to their lack of antioxidant carotenoids. In addition, the maximum growth rate was reduced, potentially due to their reduced ability to repair PSII due to lower metabolic rates. Similar responses were observed in lines that evolved to have smaller cells under nitrogen depletion. The results demonstrate that different evolutionary pathways to reduced cell size result in different changes in metabolism, with N-depleted and Small-selected cell lineages having similar sizes, but thriving differently under winter/summer conditions. With large production systems in mind, it is possible to assume that the choice of strains selected using adaptative laboratory evolution or direct selection on size can affect the overall production yield and carbon capture according to the seasons and possibly other abiotic parameters.