Dissolved organic phosphorus utilization by phytoplankton reveals preferential degradation of polyphosphates

Dissolved organic phosphorus (DOP) represents an important nutritional phosphorus (P) source for phytoplankton growth and productivity in the ocean. Polyphosphates and phosphomonoesters are dominant components of marine DOP, but the contribution of specific DOP sources to microbial community P demand is not fully understood. In a prior study, it was reported that inorganic polyphosphate was not bioavailable to the model diatoms Thalassiosira weissflogii and Thalassiosira pseudonana. However, we show that the previous finding was a misinterpretation based on a technical artifact of media preparation and that inorganic polyphosphate is actually widely bioavailable to Thalassiosira spp. In fact, orthophosphate, inorganic tripolyphosphate (3polyP), adenosine triphosphate (ATP) and adenosine monophosphate (AMP) supported equivalent growth rates and final growth yields within each of four strains of Thalassiosira spp. However, enzyme activity assays revealed that 3polyP was typically degraded more than ~10-fold faster than any other P source in these cultures. Consistent with these rate measurements, inorganic polyphosphate hydrolysis was significantly higher than P-monoester degradation rates in four of five field sites examined in the coastal western North Atlantic, which was largely driven by phytoplankton dynamics. Furthermore, targeted proteomics analysis in diatom cultures suggested that polyphosphate utilization was independent of alkaline phosphatase and may instead be driven by a number of previously unrecognized enzymes, including a putative metal-dependent inorganic pyrophosphatase. Overall, these results indicate that inorganic polyphosphates are a key bioavailable source of P for marine phytoplankton.