Widespread occurrence of phosphate storage in foraminifera might buffer anthropogenic eutrophication in coastal environments

Benthic foraminifera are a group of protists that inhabit a diverse range of habitats from salt marsh meadows to the deepest sea. Recently, benthic foraminifera have been shown to intracellularly accumulate phosphate. Intracellular phosphate concentrations can be 100-1000 times higher than in the surrounding water. Phosphate is an important macronutrient in marine ecosystems and widely used as an industrial fertilizer, which is potentially leaked to the ocean. We show that phosphate storage in foraminifera is widespread and occurs in diverse environments such as tidal flats, hypoxic fjord basins, oxygen minimum zones and the Mid-Atlantic Ridge. The highest intracellular phosphate concentrations have been found in cells of the species Ammonia confertitesta from the German Wadden Sea. The total amount of intracellular phosphate stored in A. confertitesta in the Wadden Sea during a bloom is as high as ~5% of the annual consumption of phosphorus (P)-fertilizer in Germany. More detailed budget calculations for the Southern North Sea and the Peruvian oxygen minimum zone indicate that benthic foraminifera may buffer riverine P runoff for ~37 days at the Southern North Sea and ~21 days at the Peruvian margin. This indicates that these organisms are likely relevant for marine P-cycling. They potentially buffer anthropogenic eutrophication in coastal environments.

The intracellular phosphate storage seems to have diverse functions. Coupled TEM-EDS and cryo-SEM-EDS was used to map the intracellular phosphorous distribution in cells of the species Ammonia veneta and Bolivina spissa. Phosphorous accumulations were associated with round vesicles, possibly acidocalcisomes that are typically used to store polyphosphates in eukaryotic cells. The metabolic functions of these organelles can range from regulation of osmotic pressure and intracellular pH to calcium and energy storage. Foraminifera encode the genes required for both a polyphosphate, as well as a creatine phosphate metabolism. Creatine phosphate and polyphosphates are good energy carriers that can generate energy, when electron acceptors are depleted. Thus, storage of energetic P-compounds, such as creatine phosphate and polyphosphate, is likely also an adaptation of foraminifera to O₂ depletion.