Microbial tradeoffs in internal and external use of resources regulated by phosphorus and carbon availability

A general strategy in modern agriculture to reduce phosphorus (P) fertilization is to rely on microbial efficiency of P acquisition and recycling from organic sources. However, this involves extracellular enzymes that require energy from ATP, so the process depends on the microbes’ physiological state and soil P availability. To elucidate the key relationships we compared P acquisition processes in P-poor soil (Cambisol) and links between C:P stoichiometry, enzyme activity, and ATP with microbial communities in contrasting activity states (dormancy, growth followed by starvation and gradually activated, respectively induced by no, single large (50 μg C g−1 soil) and multiple low (five days of 10 μg C g−1 soil day−1) additions of glucose as a carbon (C) source). A sole P input, without C addition, almost doubled microbial C (Cmic) contents, maintained stable phosphatase activity at 36 nmol h−1 per nmol ATP and raised microbial P (Pmic) 2.7-fold. In contrast, sole glucose addition increased Pmic by only 8%, confirming that P-limitation was much stronger than C limitation. Only 5–10 % of P potentially mineralized by phosphatase was recovered as microbial P. Cmic:Pmic ratios in microbial biomass <200 and >350 respectively reflected C starvation and strong P starvation. The ATP was a suitable predictor of microbial biomass in soil lacking fresh substrate, but weak predictor of microbial biomass after substrate input. Structural equation models revealed contrasting strategies of P utilization depending on microbial activity state. Dormant microorganisms (without glucose addition) invested most P to ATP production. In contrast, following substrate addition P-limited microorganisms accelerated phosphatase production, and hence capacity to mine P in organic sources. Thus, the P utilization/acquisition strategies depended on C accessibility and were modulated by P availability.