Phosphonate Utilization by Eukaryotic Phytoplankton: Who, How, and Where?

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Phosphorus (P) is an essential nutrient for all living cells. It is a central component of genetic material and cellular membranes and is integral to energy production and regulating enzyme activity. In the marine environment, P occurs as inorganic (Pi) and dissolved organic (DOP) forms; the availability and concentration of these different forms of P is an important control on marine phytoplankton growth. Marine phytoplankton are single-celled photosynthetic organisms and can be both prokaryotic bacteria and eukaryotic plants. While Pi is the preferred form of P for marine phytoplankton, in large regions of the oceans it is at such low levels that it restricts phytoplankton growth. In these regions, DOP is the most important P source. The composition of the DOP pool can generally be divided into two major groups: P esters and phosphonates. All marine phytoplankton are capable of using P esters to support growth; in contrast, phosphonates have only been shown to be an important source of P in the nutrition of bacteria to date. This project will determine the ability of marine eukaryotic phytoplankton to use phosphonates as a source of P for growth. Genomic analyses will determine the metabolic response of eukaryotic phytoplankton species to growth on phosphonates as well as the relevance of phosphonate use by natural populations. It is critical to understand the metabolic capabilities of phytoplankton which control marine nutrient cycling. In addition, the project is of great value in understanding the potential impacts of a changing ocean on phytoplankton growth. The project supports reseach opportunities for undergraduates from a local community college as well as hands-on enrichment programs for an afterschool program that serves a diverse student population. Comprising up to 10% of the marine DOP pool, phosphonates have been shown to be a dynamic P pool both being assimilated and produced by marine photosynthetic bacteria. The ability of eukaryotic phytoplankton to supplement their growth with phosphonates remains vastly unexplored. Several eukaryotic phytoplankton species have been shown to use glyphosate, a chemically synthesized herbicidal phosphonate, as a P source; it remains unknown if open ocean eukaryotic phytoplankton can utilize phosphonates found naturally in the marine environment. Preliminary experiments suggest at least some eukaryotic phytoplankton are able to directly utilize extracellular phosphonates. This project characterizes the pervasiveness of phosphonate utilization within eukaryotic phytoplankton lineages and identifies the cellular underpinnings that support the acquisition of and growth on naturally occuring phosphonates. The project uses whole-cell transcriptomics and functional gene complementation assays, in addition to phylogenetic analyses, to understand the bioavailability of phosphonates and relevance of phosphonate utilization by natural eukaryotic phytoplankton populations. It is critical to understand the metabolic capabilities of phytoplankton which control marine biogeochemical cycles. 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.