Regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N:P ratios

Abstract

The resilience of cyanobacterial blooms challenges lake restoration programmes based on nutrient load reduction. The survival of organisms may depend on episodic short‐term fluctuations of nitrogen (N) and phosphorus (P). Insight into physiological responses to shifts in nutrient limitation will improve our understanding of cyanobacterial bloom resilience. This study investigated the resilience and collapse of a long‐term cyanobacterial bloom dominated by Planktothrix agardhii and Raphidiopsis mediterranea, subjected to different periods of dissolved inorganic nitrogen (DIN) and phosphorus (SRP) inputs in Lago Rodó, a polymictic, hypereutrophic (6.0 ± 1.6 μmol total P/L) and turbid lake (attenuation coefficient: 4.7 ± 1.7 m−1). Phytoplankton composition, nutrient dynamics and physiological monitoring of [32P] phosphate uptake kinetics were studied over four summers. The influence of environmental nutrient supply on phytoplankton net phosphate uptake kinetics was analysed with a flow–force model that gives the threshold value of phosphate uptake ([Pe]A), a limiting concentration below which incorporation is not energetically possible by organisms, and the membrane conductivity coefficient (LP). The [Pe]A reflects the affinity and LP the activity of the cellular uptake systems. Nutrient supply into the lake sustained high DIN:SRP ratios and high cyanobacterial biomass that showed P‐deficiency features characterised by low [Pe]A (5.4 ± 0.5 nm [32P] phosphate) and high LP. High cyanobacterial biomass persisted after external nutrient inflows were interrupted for 14 months, which resulted in low dissolved DIN:SRP ratios; however, N2‐fixers did not develop. The collapse of cyanobacterial populations occurred under the lowest N:P ratios, low affinity and activity of phosphate uptake systems and strong water outflows. Our study suggests that the alleviation of N‐deficiency under high N:P ratios enhances the activation of phosphate uptake systems by cyanobacteria. The flexible physiological response results in more efficient exploitation of limiting nutrients favouring cyanobacterial resilience under suboptimal conditions.

Removal efficiency of phosphorus, cyanobacteria and cyanotoxins by the “flock & sink” mitigation technique in semi-arid eutrophic waters

“…Although studies indicate that an integrated approach is needed through the control of nitrogen (N) and phosphorus (P) (Hamilton et al, 2016), P control is considered more effective because it does not have a gas phase in the biogeochemical cycle nor are there biological mechanisms that compensate for its deficiency in a water body, unlike the fixation of atmospheric N (Xu et al, 2010;Waajen et al, 2016;Yin et al, 2016;Schindler et al, 2016). Besides that, the regulation of phosphate uptake reveals cyanobacterial bloom resilience to shifting N:P ratios, and is an efficient exploitation of limiting nutrients (Aubriot and Bonilla, 2018). Despite the importance of external sources of P in water bodies, such as those from anthropogenic activities in river basins, internal loading can contribute significantly to the total P balance and delay environmental restoration, even after reducing external loading (Lürling and van Oosterhout, 2013;Araújo et al, 2016).…”

Intra-population strain variation in phosphorus storage strategies of the freshwater cyanobacterium Raphidiopsis raciborskii

“…The duration of our study likely meant that our sampling was within the heterocyst formation lag phase for R. raciborskii. In comparison, Aubriot and Bonilla (2018) did not find N fixation in R. raciborskii cultures, even when DIN input was interrupted for 14 months. In the field, Burford et al (2014) found that the proportion of heterocyst cells in a R. raciborskii population doubled at ~13% when adding P in a mesocosm experiment in Lake Wivenhoe.…”

Mesopredator-mediated trophic cascade can break persistent phytoplankton blooms in coastal waters

“…Such outcomes can mainly be explained by the additional experimental fertilization, which supports fast-growing or grazing resistant phytoplankton. Especially cyanobacteria can exploit low pulse-wise nutrient supplies (Aubriot and Bonilla 2018) and in conjunction with small cell sizes may be grazing resistant (Lürling 2020). However, environmental daily nutrient depositional rates (see Supplement Table 1) are lower than experimentally added nutrient pulses, and usually do not occur in the form of large, pulse-wise perturbations.…”