A Novel Polyphosphate-Degrading Enzyme Confers Growth on Exogenous Polyphosphate in the Archaeon Haloferax volcanii

Polyphosphate (polyP) is an inorganic biopolymer of orthophosphate (Pi) that plays roles in many central biochemical processes in microorganisms, including acting as a cellular reservoir of phosphorus. The microbial metabolism of polyP is considered limited to its intracellular cycling by kinases and exopolyphosphatases. However, little is known about polyP metabolism in the Archaea. Notably, many haloarchaea, including Haloferax volcanii, encode homologues of bacterial polyP-synthesising genes, but lack the corresponding genes for its catabolism. Here, we show that H. volcanii possesses a novel polyP-degrading enzyme with characteristics distinguishing it from currently known enzymes. This activity also enabled H. volcanii to grow on exogenous polyP as its sole source of phosphorus. Activity was localised to a discrete protein band by native-PAGE zymography and enzyme assays of cell-free extracts from cells grown on polyP revealed the enzyme was halophilic, required Mn²⁺ or Co²⁺ and released Pi from polyP. No activity was observed in the extracellular medium of cells grown on polyP, suggesting the enzyme is either membrane-bound or intracellular. These findings thus broaden our understanding of the potential ecological roles of polyP in the biogeochemical cycling of phosphorus, and our understanding of the enzymes and pathways involved in archaeal polyP metabolism.