A widely distributed phosphate-insensitive phosphatase presents a route for rapid organophosphorus remineralization in the biosphere

• Published in: Proceedings of the National Academy of Sciences - PNAS Vol. 119; no. 5
• Main Authors: Lidbury, Ian D E A, Scanlan, David J, Murphy, Andrew R J, Christie-Oleza, Joseph A, Aguilo-Ferretjans, Maria M, Hitchcock, Andrew, Daniell, Tim J
• Format: Journal Article
• Language: English
• Published: United States National Academy of Sciences 01.02.2022
• Subjects: Bacteria; Bacterial Proteins - metabolism; Bacteroidetes; Bacteroidetes - metabolism; Bioavailability; Biodiversity; Biological activity; Biological Sciences; Biosphere; Carbohydrates; Carbon sources; Enzymes; Flavobacterium - metabolism; Growth conditions; Microbial activity; Microorganisms; Phosphatase; Phosphate; Phosphates; Phosphates - metabolism; Phosphomonoesters; Phosphoric Monoester Hydrolases - metabolism; Phosphorus; Phosphorus - metabolism; Phosphorus cycle; Regeneration; Remineralization; Substrate specificity; Substrates; Sustainable agriculture; PafA; phosphatase; Bacteroidetes; organic phosphorus; flavobacteria
• ISSN: 0027-8424; 1091-6490
• DOI: 10.1073/pnas.2118122119

The regeneration of bioavailable phosphate from immobilized organophosphorus represents a key process in the global phosphorus cycle and is facilitated by enzymes known as phosphatases. Most bacteria possess at least one of three phosphatases with broad substrate specificity, known as PhoA, PhoX, and PhoD, whose activity is optimal under alkaline conditions. The production and activity of these phosphatases is repressed by phosphate availability. Therefore, they are only fully functional when bacteria experience phosphorus-limiting growth conditions. Here, we reveal a previously overlooked phosphate-insensitive phosphatase, PafA, prevalent in , which is highly abundant in nature and represents a major route for the regeneration of environmental phosphate. Using the enzyme from , we show that PafA is highly active toward phosphomonoesters, is fully functional in the presence of excess phosphate, and is essential for growth on phosphorylated carbohydrates as a sole carbon source. These distinct properties of PafA may expand the metabolic niche of by enabling the utilization of abundant organophosphorus substrates as C and P sources, providing a competitive advantage when inhabiting zones of high microbial activity and nutrient demand. PafA, which is constitutively synthesized by soil and marine flavobacteria, rapidly remineralizes phosphomonoesters releasing bioavailable phosphate that can be acquired by neighboring cells. The gene is highly diverse in plant rhizospheres and is abundant in the global ocean, where it is expressed independently of phosphate availability. PafA therefore represents an important enzyme in the context of global biogeochemical cycling and has potential applications in sustainable agriculture.