Multifunctional alkaline phosphatases drive the phosphorus cycle in the ocean

Background Phosphorus plays a crucial role in limiting marine ecosystems productivity. To overcome this limitation, organisms use alkaline phosphatases (APases) to obtain phosphate from organic compounds. Although traditionally viewed as isoenzymes with specific roles, recent research has uncovered the multifunctionality of PhoA, a specific APase family. However, the prevalence of enzyme multifunctionality across all APase families remains unexplored, as does the determination of the dominant APases and the microbial taxa expressing them in the oceanic water column. Results Our findings revealed that all major APase families are actively expressed in the global ocean and are dominated by Alteromonas , particularly in the deep ocean. Enzymatic assays with purified recombinant APases from Alteromonas mediterranea revealed multifunctional activities with substrate affinities indicating distinct ecological roles. Proteomic analysis under phosphorus limitation unveiled specific protein regulation in Alteromonas mediterranea . Investigation into the secretion signal-peptides of APase enzymes revealed that PhoA and PafA predominantly utilize the Sec pathway for secretion, whereas PhoD and PhoX are primarily transported through the Tat pathway. Conclusions Our findings underscore the relevance of multifunctional APases in the global ocean, illustrating how microbes utilize multifunctional alkaline phosphatase families to acquire phosphorus, while ultimately highlighting the role of multifunctional enzymes in marine biogeochemical cycles.