Periphytic Microbial Response to Environmental Phosphate (P) Bioavailability and Its Relevance to P Management in Paddy Fields.

Periphyton occurs widely in shallow-water ecosystems such as paddy fields and plays a critical part in regulating local phosphorus cycling. As such, understanding the mechanisms of biofilms' response to environmental phosphate (P) variability may lead to better perceptions of P utilization and retention in rice farms. The present study aims at exploring the biological and biochemical processes underlying periphyton's P buffering capability through examining changes in community structure, phosphorus uptake and storage, and molecular makeup of the exometabolome at different levels of P availability. Under stressed (both excessive and scarce) phosphorus conditions, we found increased populations of bacterial genera capable of transforming orthophosphate to polyphosphate, as well as mixotrophic algae, that can survive through phagotrophy. These results were corroborated by observed polyphosphate buildup under low- and high-P treatment. Exometabolomic analyses further revealed that periphytic organisms may substitute sulfur (S)-containing lipids for phospholipids, use siderophores to dissolve iron (hydr)oxides to scavenge adsorbed P, and synthesize auxins to resist phosphorus starvation. These findings not only shed light on the mechanistic insights responsible for driving the periphytic P buffer but attest to the ecological roles of periphyton in aiding plants such as rice to overcome P limitations in the natural environment. IMPORTANCE The ability of periphyton to buffer environmental P in shallow aquatic ecosystems may be a natural lesson on P utilization and retention in paddy fields. This work revealed the routes and tools through which periphytic organisms adapt to and regulate ambient P fluctuation. The mechanistic understanding further implicates that the biofilm may serve rice plants to alleviate P stress. Additional results from extracellular metabolite analyses suggest the dissolved periphytic exometabolome can be a valuable nutrient source for soil microbes and plants to reduce biosynthetic costs. These discoveries have the potential to improve our understanding of biogeochemical cycling of phosphorus in general and to refine P management strategies for rice farms in particular.