Microbial physiology conserves phosphorus across long-term ecosystem development

Abstract Long-term terrestrial ecosystem development is characterized by declining soil phosphorus (P) and a corresponding increase in biological P limitation. The function of P-limited ecosystems relies on efficient use of P by soil microorganisms, but the physiological strategies used by microorganisms to manage P scarcity during ecosystem development are unknown. Here, by applying recent advances in soil metabolomic techniques to samples collected from a ~700,000-year chronosequence of ecosystem development in eastern Australia, we show that soil microbial physiological strategies for P efficiency include a high proportion of non-phosphorous membrane lipids along with substantial intracellular carbon storage. These strategies—which proliferate during primary succession and are maximized in retrogressive, P-depleted ecosystems—uphold microbial carbon limitation, triple modelled P-mineralization potential and can conserve close to double the P contained in the aboveground biomass of vegetation. These findings transform our understanding of terrestrial ecosystems by revealing a strong yet overlooked interplay between the ecophysiology of soil microorganisms and the long-term trajectory of ecosystem development.