Extraordinary physiology of polyphosphate-accumulating Beggiatoa mats suggests a key role for phosphate buffering in marine sediments

Abstract

Filamentous sulfide-oxidizing Beggiatoa spp. are widespread in marine coastal environments and can achieve significant biomass because of their substantial size. Their ability to store phosphates in the polymerized form of polyphosphates makes them potentially key players in altering the phosphorus (P) cycle at the sediment-water interface. This study examined phosphate uptake and polyphosphate formation in a P starved culture of the Beggiatoa sp. 35Flor strain. Remarkably, even after severe P starvation over five generations, the survival of the cultures was 46%, demonstrating considerable plasticity to different levels of phosphate availability. Under these P-depleted conditions, 23% of filaments still contained polyphosphates, underscoring its critical role in their metabolism. Upon reintroduction of phosphate to starved cultures, an extremely rapid phosphate uptake was observed within the first 10 minutes, with rates reaching up to 298 mmol P g-1 protein d-1, which is significantly higher than values previously described in the literature for similar-sized organisms. The high phosphate uptake capacity of Beggiatoa spp., estimated at 0.6 - 6 mmol m-2 d-1 for typical densities of filaments in coastal sediments, suggests that these bacteria may play an important role in buffering the phosphate flux in these environments. Thereby, they reduce primary production and subsequent oxygen consumption by other organisms, creating a negative feedback loop that helps maintain ecosystem stability. ImportanceSulfide-oxidizing bacteria of the genus Beggiatoa occur ubiquitously in marine coastal sediments and have a large potential to influence phosphate fluxes at the sediment-water interface owing to their ability to accumulate polyphosphate and their large size. However, the extent to which these bacteria can contribute to phosphorus (P) sequestration or release remains poorly assessed. The importance of this study lies in demonstrating the unusual flexibility in adaptation of the Beggiatoa sp. 35Flor strain to varying P availability, including extreme P starvation, and its capacity to rapidly uptake and store available phosphate in the form of polyphosphate. When considered at a global scale, these physiological traits could lead to P retention in shallow coastal waters, which, in turn, profoundly impacts ecological stability and ecosystem functioning.