Abstract
Phytoplankton face environmental nutrient variations that occur in the dynamic upper layers of the ocean. Phytoplankton cells are able to rapidly acclimate to nutrient fluctuations by adjusting their nutrient-uptake system and metabolism. Disentangling these acclimation responses is a critical step in bridging the gap between phytoplankton cellular physiology and community ecology. Here, we analyzed the dynamics of phosphate (P) uptake acclimation responses along different P temporal gradients by using batch cultures of the diatom Phaeodactylum tricornutum. We employed a multidisciplinary approach that combined nutrient-uptake bioassays, transcriptomic analysis, and mathematical models. Our results indicated that cells increase their maximum nutrient-uptake rate (Vmax) both in response to P pulses and strong phosphorus limitation. The upregulation of three genes coding for different P transporters in cells experiencing low intracellular phosphorus levels supported some of the observed Vmax variations. In addition, our mathematical model reproduced the empirical Vmax patterns by including two types of P transporters upregulated at medium-high environmental and low intracellular phosphorus levels, respectively. Our results highlight the existence of a sequence of acclimation stages along the phosphate continuum that can be understood as a succession of acclimation responses. We provide a novel conceptual framework that can contribute to integrating and understanding the dynamics and wide diversity of acclimation responses developed by phytoplankton.
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Acknowledgements
We thank the members of the Marine Resource Modeling group at Strathclyde University, specially M.R. Heath and M. Choua, for their comments on the model and our preliminary results. We would also like to acknowledge K. Griffiths for her help with 33P handling. M. W. Lomas kindly advised on the methodology for measuring P uptake. Suggestions and comments provided by James Grover and discussions with R. Anadón, F.G. Taboada, S. Romero-Romero and R. González-Gil are greatly appreciated. This research has been supported by the Marine Alliance for Science and Technology for Scotland (MASTS). C.C., S.S., and J.A.B. were supported by the Marine Alliance for Science and Technology for Scotland (MASTS) pooling initiative, funded by the Scottish Funding Council (HR09011) and contributing institutions. E.K. is grateful to the John Grieve Bequest and the Biotechnology and Biological Sciences Research Council (BBSRC) for the New Investigator Grant Award BB/M023079/1.
Funding
This research has been supported by the Marine Alliance for Science and Technology for Scotland (MASTS). C.C., S.S., and J.A.B. were supported by the Marine Alliance for Science and Technology for Scotland (MASTS) pooling initiative, funded by the Scottish Funding Council (HR09011) and contributing institutions. Gene expression experiments and analysis performed by E.K. were funded by the Biotechnology and Biological Sciences Research Council (BBSRC) (Grant Award BB/M023079/1).
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Cáceres, C., Spatharis, S., Kaiserli, E. et al. Temporal phosphate gradients reveal diverse acclimation responses in phytoplankton phosphate uptake. ISME J 13, 2834–2845 (2019). https://doi.org/10.1038/s41396-019-0473-1
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DOI: https://doi.org/10.1038/s41396-019-0473-1
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