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

Abstract

[eng] The regeneration of bioavailable phosphate from immobilizedorganophosphorus represents a key process in the global phos-phorus cycle and is facilitated by enzymes known as phosphatases.Most bacteria possess at least one of three phosphatases withbroad substrate specificity, known as PhoA, PhoX, and PhoD,whose activity is optimal under alkaline conditions. The produc-tion and activity of these phosphatases is repressed by phosphateavailability. Therefore, they are only fully functional when bacteriaexperience phosphorus-limiting growth conditions. Here, wereveal a previously overlooked phosphate-insensitive phospha-tase, PafA, prevalent inBacteroidetes, which is highly abundant innature and represents a major route for the regeneration of envi-ronmental phosphate. Using the enzyme fromFlavobacteriumjohnsoniae, we show that PafA is highly active toward phospho-monoesters, is fully functional in the presence of excess phos-phate, and is essential for growth on phosphorylatedcarbohydrates as a sole carbon source. These distinct properties ofPafA may expand the metabolic niche ofBacteroidetesby enablingthe utilization of abundant organophosphorus substrates as C andP sources, providing a competitive advantage when inhabitingzones of high microbial activity and nutrient demand. PafA, whichis constitutively synthesized by soil and marineflavobacteria, rap-idly remineralizes phosphomonoesters releasing bioavailablephosphate that can be acquired by neighboring cells. ThepafAgene is highly diverse in plant rhizospheres and is abundant in theglobal ocean, where it is expressed independently of phosphateavailability. PafA therefore represents an important enzyme in thecontext of global biogeochemical cycling and has potential appli-cations in sustainable agriculture.