期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：5
DOI：10.1073/pnas.2118122119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
At several locations across the globe, terrestrial and marine primary production, which underpin global food security, biodiversity, and climate regulation, are limited by inorganic phosphate availability. A major fraction of the total phosphorus pool exists in organic form, requiring mineralization to phosphate by enzymes known as phosphatases prior to incorporation into cellular biomolecules. Phosphatases are typically synthesized in response to phosphate depletion, assisting with phosphorus acquisition. Here, we reveal that a unique bacterial phosphatase, PafA, is widely distributed in the biosphere and has a distinct functional role in carbon acquisition, releasing phosphate as a by-product. PafA, therefore, represents an overlooked mechanism in the global phosphorus cycle and a hitherto cryptic route for the regeneration of bioavailable phosphorus in nature.
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
Bacteroidetes, which is highly abundant in nature and represents a major route for the regeneration of environmental phosphate. Using the enzyme from
Flavobacterium johnsoniae, 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
Bacteroidetes 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
pafA 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.
