Tracing the evolution of microbial alkaline phosphatases and their role in phosphorus recycling through time

Abstract

Phosphorus (P) recycling in seawater is critical for maintaining nutrient availability and marine primary productivity. This process is catalyzed by alkaline phosphatases enzymes, which hydrolyze dissolved organic phosphorus (DOP) compounds, releasing inorganic P for cellular assimilation. Here, we reconstructed the evolutionary history of three major alkaline phosphatase families through deep time using phylogenetic reconciliation across the tree of life. We further quantified their distribution and cellular localization across major metabolic groups using extant genomes to assess how the oceans capacity for P regeneration has changed through time. Our results demonstrate that alkaline phosphatases emerged early in the Archaean, indicating that DOP has sustained marine ecosystems for most of Earths history. A pronounced expansion and diversification of alkaline phosphatases occurred during the Neoproterozoic, coinciding with the rise and ecological diversification of algae. Across metabolic groups, extracellular alkaline phosphatases are particularly concentrated in ferric iron reducers, fermenters, and aerobic heterotrophs, but are comparatively rare in other metabolisms. This distribution suggests that the efficiency of marine P recycling has been strongly influenced by prevailing metabolic strategies and environmental redox conditions. Overall, our results provide new insights into the enzymatic drivers of marine P cycling and the mechanisms that maintained marine productivity as Earths surface became progressively oxygenated and biologically complex.