Award: OCE-1756271

Phosphorus (P) is an essential nutrient utilized by phytoplankton - photosynthetic, single-celled organisms that form the base of the marine food chain. Phosphorus is available in different forms and can be an important control on phytoplankton growth and their production of organic compounds from carbon dioxide, or primary production. Phytoplankton can easily transport and assimilate dissolved inorganic phosphorus (DIP), making it their preferred form of P. However, in many ocean regions DIP concentrations are consistently low. In these regions, dissolved organic phosphorus (DOP) is an important source of P. The composition of the DOP pool is complex, but can generally be divided into two major groups: P esters and phosphonates. All marine microbes, including bacteria and eukaryotic cells, are capable of utilizing P esters. In contrast, phosphonates, which can comprise up to 10% of the total DOP pool, have only been shown to be an important source of P in the nutrition of marine bacteria. The ability of eukaryotic phytoplankton to supplement growth with phosphonates remains vastly unexplored. We set out to assess the pervasiveness of phosphonate utilization within eukaryotic phytoplankton lineages as well as to characterize the cellular response of species that are able to utilize phosphonates. Of the eight species of eukaryotic phytoplankton investigated, five species were found to grow on at least one form of phosphonate as determined by an increase in cell abundance compared to cells grown under P-limiting conditions. When compared to cells given DIP, however, phosphonates were found to cause cells to grow at significantly reduced rates. Our results indicate that some eukaryotic phytoplankton can use phosphonates to support growth, however this ability is not universal, and is likely reserved for times when easier-to-assimilate forms of DOP have been exhausted. We used next-generation sequencing technologies to analyze the cellular transcriptomes of three species of eukaryotic phytoplankton given a phosphonate as the sole source of P to determine which genes are turned on or off and to what extent. We have identified several bacterial-like, phosphonate utilization genes in the eukaryotic phytoplankton transcriptomes. The presence of these genes in our target species suggests at least some eukaryotic phytoplankton may have the ability to acquire and utilize phosphonates using molecular mechanisms seen in marine bacteria. Additionally, we have identified dozens of genes of unknown function that are strongly turned on when grown under phosphonate conditions, suggesting eukaryotic phytoplankton may have novel strategies of phosphonate utilization. Finally, the transcriptomes support our findings that growth on phosphonates is stressful, as cells exhibited canonical P-limited molecular responses. The results of this project have critically enhanced our understanding of the metabolic capabilities of phytoplankton. This is especially important given the prediction that future oceans may become more stratified which could increase the importance of DOP, including phosphonates, in supporting phytoplankton growth and possibly carbon export. Thus, this study may become of great value in understanding the potential impacts of a changing ocean on ocean primary production. Last Modified: 08/15/2024 Submitted by: MichaelWLomas