A critical trade-off between nitrogen quota and growth allows Coccolithus braarudii life cycle phases to exploit varying environment

Abstract

Coccolithophores have a distinct haplo-diplontic life cycle, which allows them to grow and divide into two different life cycle phases (haploid and diploid). These life cycle phases vary significantly in inorganic carbon content and morphology and inhabit distinct niches, with haploids generally preferring low-nitrogen and high-temperature and high-light environments in situ. This niche contrast indicates different physiology of the life cycle phases, which is considered here in the context of a trait trade-off framework, in which a particular set of traits comes with both costs and benefits. However, coccolithophore’s phase tradeoffs are not fully identified, limiting our understanding of the functionality of the coccolithophore life cycle. Here, we investigate the response of the two life cycle phases of the coccolithophore Coccolithus braarudii to key environmental drivers: light, temperature, and nitrogen, using laboratory experiments. With these data, we identify the main trade-offs of each life cycle phase and use models to test the role of such trade-offs under different environmental conditions. The lab experiments show the life cycle phases have similar cell size, minimum nitrogen quotas, uptake rates, and temperature and light optima. However, we find that they have different coccosphere sizes, maximum growth rates, and maximum nitrogen quotas. We also observe a trade-off between maximum growth rate and maximum nitrogen quota, with higher growth rates and low maximum nitrogen quotas in the haploid phase and vice versa in the diploid phase. Testing these phase characteristics in a numerical chemostat model, we find that the growth–quota trade-off allows C. braarudii to exploit variable nitrogen conditions more efficiently. Because the diploid ability to store more nitrogen is advantageous when the nitrogen supply is intermittent, the higher haploid growth rate is advantageous when the nitrogen supply is constant. Although the ecological drivers of C. braarudii life cycle fitness are likely multi-faceted, spanning both top-down and bottom-up trait trade-offs, our results suggest that a trade-off between nitrogen storage and maximum growth rate is an essential bottom-up control on the distribution of C. braarudii life cycle phases.