Atypical phosphatases drive dissolved organic phosphorus utilization by phosphorus-stressed phytoplankton in the California Current Ecosystem

In the ocean, dissolved organic phosphorus (DOP) supports the health and productivity of marine phytoplankton, a phenomenon most often investigated under inorganic phosphate (Pi) scarcity. However, microbial DOP acquisition in Pi replete environments remains poorly understood. Here, we conducted a combination of nutrient addition experiments, alkaline phosphatase (AP) rate measurements, and metatranscriptomics along an onshore-to-offshore gradient in the California Current Ecosystem (CCE), an upwelling region relatively replete in Pi. We found that AP activity (APA) and eukaryotic gene transcripts for DOP utilization were present throughout the CCE. In bottle incubations, APA was upregulated in response to iron (Fe) and nitrogen (N) additions. Major contributors to these trends included atypical alkaline phosphatases (AP_aty) of diatoms in upwelling areas, and unclassified phosphodiesterases (other PDE) of multiple eukaryotic taxa in offshore regimes. APA and gene expression dynamics were not coupled to phytoplankton growth, suggesting that phytoplankton experience underlying P stress, or a state of cellular metabolism caused by Pi scarcity, even in regions primarily growth-limited by other elements. AP_atyand PDE (other) genes were highly abundant among the microbial community phosphatase pool, highlighting the importance of detecting these atypical and unclassified proteins via manual curation of metatranscriptomics data. Altogether, these results emphasize the functional diversity of phosphatases sustaining microbial community health in diverse and productive marine habitats.