Phenotypic plasticity of carbon fixation stimulates cyanobacterial blooms at elevated CO2

Abstract

Although phenotypic plasticity is a widespread phenomenon, its implications for species responses to climate change are not well understood. For example, toxic cyanobacteria can form dense surface blooms threatening water quality in many eutrophic lakes, yet a theoretical framework to predict how phenotypic plasticity affects bloom development at elevated pCO₂ is still lacking. We measured phenotypic plasticity of the carbon fixation rates of the common bloom-forming cyanobacterium Microcystis. Our results revealed a 1.8- to 5-fold increase in the maximum CO₂ uptake rate of Microcystis at elevated pCO₂, which exceeds CO₂ responses reported for other phytoplankton species. The observed plasticity was incorporated into a mathematical model to predict dynamic changes in cyanobacterial abundance. The model was successfully validated by laboratory experiments and predicts that acclimation to high pCO₂ will intensify Microcystis blooms in eutrophic lakes. These results indicate that this harmful cyanobacterium is likely to benefit strongly from rising atmospheric pCO₂.

Fig. 1. Conceptual approach of this study.

(A) Microcystis strains were grown at low and at high pCO₂ in laboratory chemostats. (Photo credit: Xing Ji, University of Amsterdam.) (B) Carbon uptake kinetics of Microcystis cells acclimated to low and high pCO₂ were measured, and (C) the plasticity of the measured uptake kinetics was incorporated in a mathematical model. (D) The model was used to predict dynamic changes in population density, uptake kinetics, and inorganic carbon chemistry, and (E) these predictions were validated by the chemostat experiments. (F) The validated model was scaled up to lakes to predict how phenotypic plasticity of Microcystis affects its bloom development in response to rising atmospheric pCO₂. This photo shows a large Microcystis bloom in Lake Taihu, China. (Photo credit: Xing Ji, University of Amsterdam.)

Fig. 2. Carbon uptake kinetics of Microcystis PCC 7806 acclimated to either low or high pCO₂.

(A and B) Net CO₂ uptake rate as function of the dissolved CO₂ concentration, after acclimation to (A) low pCO₂ and (B) high pCO₂. (C and D) Bicarbonate uptake rate as function of the bicarbonate concentration, after acclimation to (C) low pCO₂ and (D) high pCO₂. Carbon uptake kinetics were measured after ~20 days of acclimation to the steady-state conditions in the chemostats. Measurements were replicated fourfold at low pCO₂ and threefold at high pCO₂, as indicated by the different colors. Lines are Michaelis-Menten fits to each of the replicates (see table S2 for parameter estimates). Insets zoom in at the carbon uptake kinetics at low dissolved CO₂ and bicarbonate concentrations.

Fig. 3. Reaction norms of the carbon uptake kinetics of Microcystis PCC 7806 and PCC 7941.

The reaction norms show the plasticity of maximum uptake rates of (A) CO₂ (V_max,CO2,net) and (B) bicarbonate (V_max,HCO3) and the plasticity of half-saturation constants for (C) CO₂ (K_1/2,CO2) and (D) bicarbonate (K_1/2,HCO3), in response to acclimation to either low or high pCO₂. Data points show parameter values ± SD obtained by Michaelis-Menten fits to replicated measurements of the carbon uptake kinetics (see Fig. 2 and fig. S1; n = 4 for low pCO₂ and n = 3 to 4 for high pCO₂). Significant differences between parameter values at low pCO₂ and high pCO₂ were assessed using the independent-samples t test corrected for multiple hypothesis testing (***P < 0.001; *P < 0.05; n.s., not significant). Statistical details are reported in table S3.

Fig. 4. Population density, inorganic carbon chemistry, and pH in chemostat experiments with Microcystis PCC 7806 at low and at high pCO₂.

Chemostat experiments were performed in duplicate, at low pCO₂ (left) and at high pCO₂ (right). (A and B) Microcystis population density (n = 3 technical replicates per chemostat) and light intensity I_out transmitted through the chemostat (n = 10). (C and D) Dissolved CO₂, bicarbonate, and carbonate concentrations. (E and F) Dissolved inorganic carbon (DIC) and pH (n = 3 technical replicates per chemostat). Symbols indicate experimental data of the duplicate chemostat experiments, error bars indicate SDs of technical replicates, and lines indicate model predictions. Error bars in (E) and (F) did not exceed the size of the symbols. For comparison, gray lines in (A) and (B) are model predictions for nonacclimated cells that either (A) grow at low pCO₂ but with carbon uptake kinetics acclimated to high pCO₂ or (B) grow at high pCO₂ but with carbon uptake kinetics acclimated low pCO₂. Steady-state characteristics of the experiments are summarized in table S1, and parameter values of the model are listed in tables S4 and S5.

Fig. 5. Microcystis blooms predicted for lakes with different atmospheric pCO₂ and alkalinity.

(A to D) Model predictions of (A) cyanobacterial population density, (B) dissolved CO₂ concentration, bicarbonate, and pH, (C) maximum net CO₂ uptake rate, and (D) half-saturation constant for bicarbonate uptake in Microcystis blooms of eutrophic lakes at different atmospheric pCO₂ and an alkalinity of 1 mEq liter⁻¹. Predictions were made for three phenotypes: a plastic phenotype (green line), a low pCO₂ phenotype (dashed gray line), and a high pCO₂ phenotype (solid gray line). (B) Predictions only for the plastic phenotype. (E) Contour plot of the population density of the plastic phenotype, predicted for eutrophic lakes with different atmospheric pCO₂ and alkalinity. Black lines indicate the parameter regions at which the carbon uptake kinetics of the plastic phenotype have almost fully adjusted (≥90%) to either low pCO₂ or high pCO₂. The arrow indicates the transition zone where the plastic phenotype shifts from low pCO₂ to high pCO₂ uptake kinetics. All graphs show model predictions for cyanobacterial blooms at steady state. Species and lake parameters are provided in tables S5 and S6.