Shedding light on the paradox of high alkaline phosphatase utilization at high end-product concentrations

Alkaline phosphatase (APase) activity is supposed to be regulated by the concentration of its endproduct, decreasing with increasing inorganic phosphate (Pi) concentrations. Since Pi is readily available in the deep ocean, APase activity would be expected to be low. However, high APase activities at high Pi concentrations have been found in the deep Indian and Atlantic Ocean. To understand how APase activities are regulated and what mechanisms are responsible for its regulation we performed microcosm experiments with mesopelagic North Atlantic waters. Treatments consisted of enrichment with either ammonium or organic carbon, and were compared to unamended controls. We assessed changes in prokaryotic abundance, APase, leucine aminopeptidase, heterotrophic production, dark CO₂ fixation and community gene expression (metatranscriptomics) between treatments and control. In the organic matter enrichments, APase increased along with all measured rates, whereas only dark CO₂ fixation and APase were enhanced in the ammonium enrichment. In the organic matter enrichment, genes for heterotrophic metabolism were strongly upregulated, whereas genes for ammonia oxidation and CO₂ fixation were upregulated in the ammonium treatment. In both treatments, the Pho regulon –a global regulatory mechanism involved in bacterial Pi management– was also upregulated, including genes encoding alkaline phosphatases. The activation of the Pho regulon seemed to be related to cross-activation by nonpartner histidine kinases, and/or the activation of genes involved in the regulation of elemental balance during catabolic processes. Increased C or N bioavailability thus appear to elicit a Pi deficiency inside cells and activate the Pho regulon. These results indicate possible ways (e.g. pulses of C or N or changes in elemental ratios) in which APase can be activated irrespectively of the environmental Pi concentration.