Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake

Carlos Caceres, The Ohio State University, School of Environment and Natural Resources, Columbus, OH, United States, Sofie Spatharis, University of Glasgow, College of Medical, Veterinary & Life Sciences, Glasgow, United Kingdom, Eirini Kaiserli, University of Glasgow, Institute of Biodiversity, Animal Health and Comparative Medicine, Glasgow, United Kingdom, Evangelia Smeti, Hellenic Centre for Marine Research, Biological Resources and Inland Waters, Greece, Hugh Flowers, School of Chemistry, University of Glasgow, Glasgow, United Kingdom and Juan A Bonachela, Rutgers University, Department of Ecology, Evolution, and Natural Resources, United States
Phytoplankton cells are able to adjust their nutrient uptake machinery and metabolism to face nutrient variations that occur in aquatic environments. Disentangling these phenotypic changes (i.e. acclimation responses) is a critical step in bridging the gap between phytoplankton cellular physiology, community ecology, and ecosystem functioning. In this study, we applied a multidisciplinary approach that combined nutrient uptake bioassays, transcriptomic analysis, and mathematical models to investigate the dynamics of phosphate uptake acclimation responses. Our experiments monitored the physiological changes in a population of the diatom Phaeodactylum tricornutum subject to phosphate pulses of three different magnitudes. We found an increase in the maximum phosphate-uptake rate (Vmax) both after nutrient pulses and at low phosphate levels, and a decrease at intermediate nutrient levels. Furthermore, the three genes analyzed coding for P transporters were upregulated in cells experiencing low intracellular phosphorus levels. Our mathematical model reproduced the empirical Vmax patterns by including two types of P transporters upregulated at different phosphorus levels, and highlighted the existence of a sequence of acclimation stages along the phosphate continuum. Our study provides a novel conceptual framework that contributes to integrating and understanding the wide diversity of acclimation responses developed by phytoplankton. This framework could be accommodated to other organisms and resources, since nutrient uptake acclimation responses are ubiquitous in kingdoms Monera, Protist, and Fungi.