Surface-adsorbed phosphorus buffers environmental phosphate availability and influences phosphorus uptake in Chlamydomonas reinhardtii

Phosphorus is a key driver of eutrophication in aquatic ecosystems, and microalgae play a central role in regulating environmental phosphate availability through uptake and retention processes. Although intracellular polyphosphate accumulation has been intensively studied, the contribution of cell surface-adsorbed phosphorus (SAP) to environmental P capture remains poorly understood. Here, using Chlamydomonas reinhardtii as a model, we show that under standard growth conditions, cell wall-intact strains accumulated significantly more SAP (~2-fold) than wall-deficient strains, with SAP levels increasing linearly with external Pi. Although SAP accounted for less than 15% of total cellular P, overall P content was up to ~1.8-fold higher in cell wall-intact strains under Pi-replete conditions. Genetic manipulation of the Pi starvation regulator PSR1 further reshaped P partitioning. PSR1 overexpression increased intracellular P accumulation by ~66%, whereas PSR1 disruption elevated SAP (>67%) but reduced total P (~28%), accompanied by diminished Pi removal from the medium. In addition, carbon limitation markedly reduced genotypic differences in SAP accumulation, indicating that surface retention is metabolically constrained rather than solely determined by structural features. Together, these findings indicate that SAP formation arises from PSR1-dependent P partitioning dynamics and represents a transient, regulated interfacial pool rather than an independently controlled adsorption process. While intracellular storage remains the dominant P sink, SAP functions as a dynamic and exchangeable buffer at the cell-water interface, facilitating P retention prior to internalization. This work provides a mechanistic framework linking cell surface processes with intracellular accumulation, advancing our understanding of how microalgae buffer fluctuating P availability and regulate P uptake dynamics in aquatic environments.