Journal Article

Structural Evolution of Bacterial Polyphosphate Degradation Enzyme for Phosphorus Cycling

Zhang, Dong, Hua, Yuejin, Huang, Cheng, Zhang, Furong, Zhou, Ruhong, Xie, Zhenming, Cai, Chunhui, Zhao, Ye, Wang, Binqiang, Tian, Bing, Ye, Rui, Yu, Ning, Zhao, Jie, Dai, Shang

2024

Overview

Living organisms ranging from bacteria to animals have developed their own ways to accumulate and store phosphate during evolution, in particular as the polyphosphate (polyP) granules in bacteria. Degradation of polyP into phosphate is involved in phosphorus cycling, and exopolyphosphatase (PPX) is the key enzyme for polyP degradation in bacteria. Thus, understanding the structure basis of PPX is crucial to reveal the polyP degradation mechanism. Here, it is found that PPX structure varies in the length of ɑ‐helical interdomain linker (ɑ‐linker) across various bacteria, which is negatively correlated with their enzymatic activity and thermostability – those with shorter ɑ‐linkers demonstrate higher polyP degradation ability. Moreover, the artificial DrPPX mutants with shorter ɑ‐linker tend to have more compact pockets for polyP binding and stronger subunit interactions, as well as higher enzymatic efficiency (kcat/Km) than that of DrPPX wild type. In Deinococcus‐Thermus, the PPXs from thermophilic species possess a shorter ɑ‐linker and retain their catalytic ability at high temperatures (70 °C), which may facilitate the thermophilic species to utilize polyP in high‐temperature environments. These findings provide insights into the interdomain linker length‐dependent evolution of PPXs, which shed light on enzymatic adaption for phosphorus cycling during natural evolution and rational design of enzyme. This study demonstrates an interdomain linker‐based exopolyphosphatase (PPX) structural evolution in bacteria. The length of ɑ‐linker in PPX, which involves phosphate cycling, is varied among bacteria and has impacts on protein's conformation and quaternary structure, thus posing an impact on enzyme activity and thermostability. These results suggest a potential relationship between PPX structural evolution and bacterial environmental adaptability.

• Publisher: John Wiley & Sons, Inc,John Wiley and Sons Inc,Wiley
• Subject: Acid Anhydride Hydrolases - chemistry / Acid Anhydride Hydrolases - genetics / Acid Anhydride Hydrolases - metabolism / Amino acids / Bacteria / Bacteria - enzymology / Bacteria - genetics / Bacteria - metabolism / Chromatography / E coli / Enzymes / Evolution, Molecular / exopolyphosphatase / Kinases / Metabolism / Phosphorus - metabolism / polyphosphate / Polyphosphates - metabolism / Proteins / structural evolution / ɑ‐linker