Energetic and Metabolic Costs of Organic Phosphorus Mineralization in Microbial Hotspots

Phosphorus (P) is essential for life but is often poorly available to plants, limiting biological processes in ecosystems. Microbial transformations increase P availability through enzymatic hydrolysis of organic P compounds; however, these processes are metabolically and energetically costly and occur predominantly in microbial hotspots, such as the rhizosphere and other microsites with elevated microbial activity. Microorganisms invest cellular energy, primarily in the form of ATP, to produce phosphatase enzymes required for P mineralisation.

This study aimed to quantify the energetic and metabolic costs of enzymatic hydrolysis of organic P compounds of increasing complexity within microbial hotspots. We hypothesized that (i) energy investment for enzyme production increases with substrate complexity and its interaction with soil minerals, and (ii) enzyme-mediated P mineralization requires higher energy input than direct P uptake. To test these hypotheses, a soil–sand mixture was incubated with different P substrates while measuring heat dissipation (microcalorimetry), enzyme activities, soil ATP content, and available P.

Four treatments were applied: inorganic P (control), glycerol phosphate, DNA, and phytic acid (phytate). Heat release increased with substrate complexity, from phosphomonoester to DNA, indicating higher energetic investment. Microorganisms invested more energy in enzyme production than in P uptake, and phosphomonoesterase activity increased with substrate complexity. In contrast, phosphodiester hydrolysis was constrained by low phosphodiesterase activity, reflecting higher metabolic costs.

These results demonstrate that microbial hotspot activity governs the energetic efficiency of organic P transformations in soils, highlighting the importance of microscale processes for soil P cycling.

Acknowledgments and Funding: This work was funded by the German Research Foundation (DFG, BI 2570/1-1), project number 525137622.