Phytate as a Phosphorus Nutrient with Impacts on Iron Stress-Related Gene Expression for Phytoplankton: Insights from the Diatom Phaeodactylum tricornutum

Phytoplankton have evolved a capability to acquire phosphorus (P) from dissolved organic phosphorus (DOP) since the preferred form, dissolved inorganic phosphate (DIP, or Pi), is often limited in parts of the ocean. Phytic acid (PA) is abundantly synthesized in plants and rich in excreta of animals, potentially enriching the DOP pool in coastal oceans. However, whether and how PA can be used by phytoplankton are poorly understood. Here, we investigated PA utilization and underlying metabolic pathways in the diatom model Phaeodactylum tricornutum. The physiological results showed that P. tricornutum could utilize PA as a sole source of P nutrient to support growth. Meanwhile, the replacement of PA for DIP also caused changes in multiple cellular processes, such as inositol phosphate metabolism, photosynthesis, and signal transduction. These results suggest that PA is bioavailable to P. tricornutum and can directly participate in the metabolic pathways of PA-grown cells. However, our data showed that the utilization of PA was markedly less efficient than that of DIP, and PA-grown cells exhibited P and iron (Fe) nutrient stress signals. Implicated in these findings is the potential of complicated responses of phytoplankton to an ambient DOP species, which calls for more systematic investigation. IMPORTANCE PA is abundant in plants and cannot be digested by nonruminant animals. Hence, it is potentially a significant component of the DOP pool in coastal waters. Despite this potential importance, there is little information about its bioavailability to phytoplankton as a source of P nutrient and the molecular mechanisms involved. In this study, we found that part of PA could be utilized by the diatom P. tricornutum to support growth, and another portion of PA can act as a substrate directly participating in various metabolism pathways and cellular processes. However, our physiological and transcriptomic data show that PA-grown cells still exhibited signs of P stress and potential Fe stress. These results have significant implications in phytoplankton P nutrient ecology and provide a novel insight into multifaceted impacts of DOP utilization on phytoplankton nutrition and metabolism.

Automated summary

Phytoplankton have the capability to acquire phosphorus from dissolved organic phosphorus, and can use phytic acid as a source of phosphorus nutrient. However, the utilization efficiency of phytic acid is lower compared to dissolved inorganic phosphate, and can lead to nutrient stress signals in cells.