The combined effects of pCO2 and nitrogen conditions on the growth and carbon acquisition of the freshwater cyanobacterium Microcystis aeruginosa.

Abstract

Elevated CO2 concentrations in freshwater ecosystems, driven by the anthropogenic increase of atmospheric pCO2, may affect the growth, stoichiometry and carbon acquisition of phytoplankton. The direction and extent of these changes may be dependent on other environmental factors, such as nutrient loads. In this study we investigated the response of three strains of the freshwater cyanobacterium, Microcystis aeruginosa, to a wide range of pCO2 under replete and deplete nitrogen conditions, in order to investigate their combined effects. This species is known in particular to cause intensive harmful blooms during warm periods in eutrophic systems. These blooms can deplete CO2 concentrations to limiting conditions and may therefore be promoted by increased CO2 availability. We found for all strains that increased pCO2 affects C:N ratios and that the direction and extent of the response is dependent on the imposed nitrogen conditions. Specifically, C:N ratios increased with pCO2 under nitrogen depleted conditions, while they decreased under nitrogen replete conditions. Furthermore, we found impaired growth rates at both low pCO2 and at high pCO2. This may be closely related to changes in carbon acquisition or putative photoinhibition. Changes in carbon acquisition are investigated using a single compartment model for stable carbon isotope fractionation (εp). Microcystis generally takes up bicarbonate as secondary carbon source. With εp calculations it is shown that cells become less reliant on bicarbonate at high pCO2 and take up more CO2 instead. The calculations also show that the total carbon uptake increases with increasing pCO2 in nitrogen limited conditions. This is closely related to an increase in CO2 leakage from cells at high pCO2. These changes in carbon acquisition may have consequences for the growth and the energy balance of cells. Next to being a useful tool to track changes in carbon acquisition, the relation between pCO2 and εp is also of particular interest for the reconstruction of past pCO2. εp has been shown to increase with increasing pCO2. This response interacts with the imposed nitrogen conditions, leading to a higher sensitivity to pCO2 during nitrogen depleted than in nitrogen replete conditions. The observed strong relationship between εp and pCO2 may support the development of CO2 proxies, though this will be complicated by the interactive effect with nitrogen conditions. This study highlights the changes that occur at a physiological level in response to elevated pCO2 under nitrogen replete/deplete conditions. The results show that elevated pCO2 may promote Microcystis growth when it alleviates CO2 limitation, but that it may impede growth when it becomes saturating. Large changes in C:N stoichiometry indicate a large flexibility of cyanobacteria. If the physiological changes observed in this study provide an ecological advantage for cyanobacteria it may have implications for the phytoplankton community composition. In all, the impacts of elevated pCO2 on cyanobacterial blooms will strongly depend on the concurrent CO2 and nitrogen concentrations, which may strongly influence the success of cyanobacteria in future freshwater ecosystems.