Biogenic phosphonate utilization by globally distributed diatom Thalassiosira

Phosphonate is a class of enigmatic organic phosphorus compounds that contribute [~]25% of total dissolved organic phosphorus (DOP). Recent studies reveal the important role of phosphonate mediated by prokaryotes in the marine P redox cycle, however, its bioavailability and metabolic process by eukaryotic phytoplankton are under debate. 2-Aminoethylphosphonic acid and (2-AEP) and 2-amino-3-phosphonopropionic acid (2-AP3) are two biogenic phosphonates that ubiquitously exist in marine environment. Here, we report that Thalassiosira pseudonana, a dominant diatom species in the ocean, are able to recover growth from phosphorus starvation with individual supplement of 2-AEP and 2-AP3. Moreover, the cellular stoichiometric C:P and N:P ratios of cells grown under 2-AEP are in-between the P-depleted and DIP-replete groups. This study provided evidence that biogenic phosphonates can be adopted as alternative phosphorus sources to support diatom growth and might have a profound effect on the elemental stoichiometry in the oligotrophic ocean. Scientific significance statementPhosphorus (P) is a major limiting macronutrient for primary productivity in the ocean, whilst the biologically mediated cycling of different P forms is less understood compared to carbon and nitrogen. Accounting for 25% of the marine dissolved organic phosphorus pool, phosphonate bioavailability by eukaryotic phytoplankton still remains discrepancies. In line with our hypothesis, here we report that a cosmopolitan diatom Thalassiosira pseudonana can utilize biogenic phosphonates 2-aminoethylphosphonic acid and 2-amino-3-phosphonopropionic acid to support cell growth, with deviated cellular C:N:P in comparison to that of P-replete cells. Furthermore, cells grown under lower temperature exhibit physiological adaptation (K-selection strategy) with the benefit of 2-AEP supplied in the medium. We provide the evidence that utilization of biogenic phosphonate is ubiquitous in diatom and it might have profound effect on elemental stoichiometry ratios in the environment. Filling in this missing puzzle piece provides us with a fresh perspective to elucidate the role of phosphonates in marine phosphorus cycle and biological pump.