Distinctive physiology of polyphosphate-accumulating Beggiatoa suggests an important role in benthic phosphorus cycling

Abstract

Filamentous sulfide-oxidizing Beggiatoa spp., which occasionally form extensive white microbial mats, are widespread in marine coastal environments and can achieve significant biomass because of their large size. Their ability to store phosphates in the polymerized form of polyphosphates makes them potential 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 Beggiatoa sp. 35Flor strain. Remarkably, even after sustained P starvation over five generations, the mat establishment rate of the examined culture was 46%, demonstrating considerable plasticity in response to different levels of phosphate availability. Under these P-depleted conditions, at least 17% of filaments still contained polyphosphates, highlighting their critical role in their metabolism. Upon reintroduction of phosphate to starved cultures, an extremely rapid phosphate uptake was observed within the first 10 min, with rates reaching up to 12.4 mmol phosphate g^-1 protein h^-1, which is significantly higher than values previously reported 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 under certain environmental conditions, these bacteria could act as a P sink and thus play an important role in benthic P cycling.

Importance: Sulfide-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 remarkable flexibility in the adaptation of the strain Beggiatoa sp. 35Flor to varying P availability, including prolonged P starvation and its capacity to rapidly uptake and store available phosphate in the form of polyphosphate. When considered on a global scale, these physiological traits could form the basis for Beggiatoa's role in moderating P fluxes.

Keywords: coastal ocean; marine sediments; phosphate starvation; phosphate uptake; polyphosphate; sulfur bacteria.

Fig 1

Schematic of the experimental design used in this study. (A) Phosphorus starvation over five generations. Each generation was cultivated for 6 days, with a specified amount of culture transferred to fresh sterile media (inoculum volume). During each cultivation attempt, an average of 10 tubes were inoculated per generation. This process was repeated across multiple cultivation attempts (blue), leading to variations in the total number of tubes (red) inoculated per generation. (B) Phosphate incubation experiment. Phosphate uptake experiment was performed on the fifth generation of P-starved cultures. During each incubation, samples were taken before phosphate addition to the mat (time 0) and after 10 min, 30 min, 2 h, and 24 h of incubation. The experiment was repeated five times using a new set of cultivation tubes. This resulted in 30 culture tubes being sacrificed for each of the five separate incubation experiments.

Fig 2

Mat establishment rate of P-starved Beggiatoa sp. 35Flor cultures over five generations. Boxes show the first and third quartiles; horizontal line: median; whiskers: 1.5 times the interquartile range from the edges of the box; dots represent outliers. n indicates the number of independent cultivation attempts, with each involving an average of 10 inoculated tubes. t is the total number of tubes inoculated per generation during the experiment. Letters (a and b) indicate significant differences (Dunn’s test, BH-adjusted P-value < 0.05).

Fig 3

Polyphosphate dynamics in Beggiatoa sp. 35Flor following the addition of phosphate to the P-starved cultures. (A) Percentage of filaments containing polyphosphates (indicated as yes/no) over the course of the experiment; error bars show the standard deviation (n = 5). (B–E) DAPI-stained fluorescence images of Beggiatoa sp. 35Flor cultures at different times of incubation: (B) P-starved culture at the beginning without P-addition (time 0), and (C) after 30 min, (D) after 2 h, and (E) after 24 h of incubation with P. Bars represent 10 µm.

Fig 4

Concentrations of dissolved inorganic phosphate (A) and particulate P (B) over incubation time. Each dot represents a measurement from each of the five iterations of the experiment. The black line shows the fitted curve, and the gray ribbon shows the 95% CI for the fitted curve.