Polyphosphate as an Integral Component of Global Phosphorus Cycling through Earth's History

Polyphosphate (polyP), a condensed linear form of orthophosphate residues, is functionally versatile phosphorus (P) polymer that has persisted since prebiotic Earth. Long treated as a cellular biochemical curiosity, it remains systematically overlooked in global P budgets and Earth system models. In this review, we compile the first global-scale synthesis of environmental occurrence, biological regulation, and ecosystem functions of polyP across terrestrial, freshwater, marine, and engineered systems. Integrating 568 environmental observations and over 3000 microbial genomes, we unveil that polyP is a quantitatively significant and phylogenetically widespread component of global P cycling, often comprising 5-40% of total phosphorus in major ecosystems. We synthesize current understanding of how microbial taxa, including bacterial or archaeal polyP-accumulating organisms and arbuscular mycorrhizal fungi, mediate polyP turnover and interact with carbon/nitrogen cocycling under fluctuating redox, nutrient, and climatic conditions. Our quantitative assessment reveals that global polyP stocks in soils, sediments, and wastewater systems form a substantial, yet previously unaccounted, reservoir of recoverable and climate-sensitive P. The omission of polyP from existing models creates systematic blind spots in understanding P bioavailability, retention, cycling, and sustainability. Integrating polyP into the global P narrative is essential for advancing new frontiers in climate-smart biogeochemical forecasts, circular nutrient management, and long-term water-energy-food ecosystem security under global climate change.