Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility

Cyanobacterial mats inhabit a variety of aquatic habitats, including the most extreme environments on Earth. They can thrive in a wide range of phosphorus (P) levels and are thus important players for ecosystem primary production and P cycling at the sediment-water interface. Polyphosphate (polyP), the major microbial P storage molecule, is assigned a critical role in compensating for phosphate fluctuations in planktonic cyanobacteria, but little is known about potentially analogous mechanisms of mat-forming cyanobacteria. To investigate acclimation strategies of cyanobacterial mats to fluctuating phosphate concentrations, laboratory batch experiments were conducted, in which the cosmopolitan mat-forming, marine cyanobacterium Sodalinema stali was exposed to low dissolved P concentrations, followed by a P pulse. Our results show that the cyanobacteria dynamically adjusted cellular P content to ambient phosphate concentrations and that they had accumulated polyP during periods of high phosphate availability, which was subsequently recycled to sustain growth during phosphate scarcity. However, following the depletion of dispensable cellular P sources, including polyP, we observed a reallocation of P contained in DNA into polyP, accompanied by increasing alkaline phosphatase activity. This suggests a change of the metabolic focus from growth towards maintenance and the attempt to acquire organic P, which would be naturally contained in the sediment. P overplus uptake following a simulated P pulse further suggests that Sodalinema-dominated mats exhibit elaborated mechanisms to cope with severe P fluctuations to overcome unfavourable environmental conditions, and potentially modulate critical P fluxes in the aquatic cycle.