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

Abstract

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 occurring in Pi replete ocean environments remains poorly understood. Here, we conducted a combination of nutrient addition experiments, alkaline phosphatase (AP) rate measurements, and metatranscriptomics analyses along an onshore-to-offshore gradient in the California Current Ecosystem (CCE), a relatively Pi-rich upwelling region. We found that AP activity (APA) and eukaryotic 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 (APaty) of diatoms in the coastal upwelling area, and unclassified non-cytoplasmic P-diesterases (PDEnc) of multiple eukaryotic taxa in the offshore regime. APA and gene expression dynamics were not coupled to phytoplankton growth, suggesting that these organisms experience underlying P stress, a state of cellular metabolism caused by Pi scarcity, even in regions primarily growth-limited by other elements. While APaty and PDEnc were highly abundant among the microbial community phosphatase pool, these genes were missing from a widely used annotation database, highlighting the importance of manual curation for the detection of these atypical and unclassified proteins. Altogether, these results emphasize the functional diversity of phosphatases sustaining microbial community health in diverse and productive marine habitats.