Resolving the paradox: Continuous cell-free alkaline phosphatase activity despite high phosphate concentrations

It is generally recognised that enzymatic activities are controlled by their end-product concentration, so that when the end-product concentration is high the enzyme activity is low and vice versa. In the marine environment, however, high alkaline phosphatase (APase) activities at high inorganic phosphorus (P-i) concentrations are commonly observed. This represents a paradox that has been unresolved for decades. This study builds on recent advances in the understanding of the role of cell-free versus cell-associated extracellular enzymatic activities (EEAs) to find an explanation for this long-time enigma. Data was collected from coastal (biweekly for 1 y), epi-and mesopelagic waters open-ocean (bimonthly for 9 months) and lab experiments to investigate the relation between APase (cell-free and cell-associated) and P-i. The proportion of cell-free APase was consistently high across all these marine environments (ranging from 65 to 100% of the total activity), irrespective of the P-i concentration. A residence times experiment performed with APase enzymes from the same marine environment confirmed that cell-free APase maintained most of its activity (ca. 75% of the initial in situ activity) over a 16-day incubation. This demonstrates the long lifetime of APase in the marine environment, and the potential for spatial and temporal decoupling between the P-i concentrations and the total APase activity. Collectively, these results together with previous evidence, suggest that the persistent presence of cell-free APase activity provides a reasonable explanation for the paradox of high potential APase activities at high end-product (P-i) concentration in the marine environment. Ultimately, this finding also serves as an example of the potential critical role that cell-free enzymes play in the ecology and biogeochemistry of the ocean.