Redox chemistry in the phosphorus biogeochemical cycle

Abstract

The element phosphorus (P) controls growth in many ecosystems as the limiting nutrient, where it is broadly considered to reside as pentavalent P in phosphate minerals and organic esters. Exceptions to pentavalent P include phosphine--PH3--a trace atmospheric gas, and phosphite and hypophosphite, P anions that have been detected recently in lightning strikes, eutrophic lakes, geothermal springs, and termite hindguts. Reduced oxidation state P compounds include the phosphonates, characterized by C-P bonds, which bear up to 25% of total organic dissolved phosphorus. Reduced P compounds have been considered to be rare; however, the microbial ability to use reduced P compounds as sole P sources is ubiquitous. Here we show that between 10% and 20% of dissolved P bears a redox state of less than +5 in water samples from central Florida, on average, with some samples bearing almost as much reduced P as phosphate. If the quantity of reduced P observed in the water samples from Florida studied here is broadly characteristic of similar environments on the global scale, it accounts well for the concentration of atmospheric phosphine and provides a rationale for the ubiquity of phosphite utilization genes in nature. Phosphine is generated at a quantity consistent with thermodynamic equilibrium established by the disproportionation reaction of reduced P species. Comprising 10-20% of the total dissolved P inventory in Florida environments, reduced P compounds could hence be a critical part of the phosphorus biogeochemical cycle, and in turn may impact global carbon cycling and methanogenesis.

Keywords: biogeochemistry; element cycling; phosphonates; phosphorus; redox chemistry.

Fig. 1.

Phosphorus compounds with proposed transformations denoted by arrows. Oxidation state is shown above.

Fig. 2.

HPLC-ICP-MS spectrum of water from central Florida (River Front Park B-3-g, Tampa) showing hypophosphite (∼0.8 min), phosphite (∼7 min), and phosphate (∼14 min) peaks. The concentration of each P species was estimated from the peak height using standards with concentrations of 10⁻⁷ M, 5 × 10⁻⁷ M, 10⁻⁶ M, 5 × 10⁻⁶ M, and 10⁻⁵ M of each P species. Peak heights varied linearly with concentration (R² = 0.999, 0.9996, and 0.998 for hypophosphite, phosphite, and phosphate, respectively), and the linear relationship between concentration and peak height was used to calculate individual P species concentration. Both reduced P compounds combined comprise about 26% of the total P (0.2 mg/L) in this sample.

Fig. 3.

Modeled phosphine atmospheric concentration calculated with respect to percent of total dissolved inorganic P as phosphite in freshwater, with the remainder phosphate. These calculations calculate the quantity of phosphine in air (ng/m³) resulting from disproportionation of phosphite (reaction 1), which is dependent on pH, temperature, amount of P as phosphite, and total P. (A) Dependence on PH₃ concentration on total phosphorus in solution, with constant temperature and pH. (B) Dependence on pH. (C) Dependence on temperature.

Fig. 4.

Contour plot illustrating PH₃ atmospheric concentration (ng/m³) dependence on phosphite and hypophosphite activity in water, assuming a pH of 7.2, temperature of 298 K, and total free dissolved inorganic phosphate activity of 10⁻⁶. PH₃ abundance is solved for using the HSC chemistry program (see Methods) and follows predictions from reactions 1 and 2. The phosphite and hypophosphite concentrations from Fig. 2 would be in equilibrium with between 1 and 10 ng/m³ of phosphine, consistent with the measured PH₃ concentrations from the Florida Everglades (52).