Microbial phosphorus recycling in soil by intra- and extracellular mechanisms

Rising global stoichiometric imbalance between increasing nitrogen (N) availability and depleting phosphorus (P) resources increases the importance of soil microbial P recycling. The contribution of extra- versus intracellular P (re-)cycling depending on ecosystem nutrient status is vastly unclear, making soil microorganisms a blind spot in our understanding of ecosystem responses to increasing P deficiency. We quantified P incorporation into microbial DNA and phospholipids by 33P labeling under contrasting conditions: low/high P soil × low/high carbon (C)NP application. By combining 33P and 14C labeling with tracing of microbial community biomarkers and functional genes, we disengaged the role of DNA and phospholipids in soil P cycling. Microorganisms in low P soil preferentially allocated P to phospholipids with an acceleration of phospholipids metabolism driven by C addition, which was strongly related to high abundances of microbial community members (e.g. some G-) with a fast phospholipids turnover. In high P soil, however, more P was allocated to DNA with a microbial functional shift towards DNA synthesis to support a replicative growth when sufficient C was supplied, which was coupled with a strong enrichment of fungal copiotrophs and microbial genes coding DNA primase. Consequently, adaptation to low P availability accelerated microbial intracellular P recycling through reutilization of the P stored in phospholipids. However, microorganisms under high P availability commonly adopted extracellular P recycling with release and reuse of DNA P by microbial death-growth dynamics. These results advance our understanding on microbial adaptation to P deficiency in soil by regulating component-specific P pathways and reflect the specific functions of phospholipids and DNA for P recycling.