Date Published: March 22, 2017
Publisher: Public Library of Science
Author(s): Sajeela Ghaffar, R. Jan Stevenson, Zahiruddin Khan, Jean-François Humbert.
This study was designed to advance understanding of phosphorus regulation of Microcystis aeruginosa growth, phosphorus uptake and storage in changing phosphorus (P) conditions as would occur in lakes. We hypothesized that Microcystis growth and nutrient uptake would fit classic models by Monod, Droop, and Michaelis-Menten in these changing conditions. Microcystis grown in luxury nutrient concentrations was transferred to treatments with phosphorus concentrations ranging from 0–256 μg P∙L-1 and luxury nitrogen. Dissolved phosphorus concentration, cell phosphorus quota, P uptake rate and cell densities were measured at day 3 and 6. Results showed little relationship to predicted models. Microcystis growth was asymptotically related to P treatment from day 0–3, fitting Monod model well, but negatively related to P treatment and cell quota from day 3–6. From day 0–3, cell quota was negatively related to P treatments at <2 μg∙L-1, but increased slightly at higher P. Cell quota decreased greatly in low P treatments from day 3–6, which may have enabled high growths in low P treatments. P uptake was positively and linearly related to P treatment during both periods. Negative uptake rates and increases in measured culture phosphorus concentrations to 5 μg∙L-1 in the lowest P treatments indicated P leaked from cells into culture medium. This leakage during early stages of the experiment may have been sufficient to stimulate metabolism and use of intracellular P stores in low P treatments for rapid growth. Our study shows P regulation of Microcystis growth can be complex as a result of changing P concentrations, and this complexity may be important for modeling Microcystis for nutrient and ecosystem management.
Freshwater harmful algal blooms, often dominated by cyanobacteria, are speculated to increase with climate change and are expected to decrease the potable and recreational uses of water [1–2]. Microcystis aeruginosa (referred to as “Microcystis” in this paper for convenience) is a common constituent of harmful cyanobacterial blooms [3–5]. Many strains of Microcystis produce microcystin, a hepatotoxin, which enters the food chain and disrupts ecological balance  and is a human health hazard . Thus, Microcystis has been a big problem and has been studied worldwide in freshwater ecosystems [8–11].
Variability in phosphorus concentrations within P treatment was relatively low and clearly showed effects of P treatment (Fig 1), with potential leakage of phosphorus in low P treatments and phosphorus uptake in high P treatments. Phosphorus concentrations in cultures on day 3 averaged about 5 μg L-1 and varied little among P treatments ranging from 0 to 16. Phosphorus concentrations in cultures on day 3 increased steadily from 5 to 115 μg L-1 with P treatments from 16 to 256. Phosphorus concentrations in cultures on day 6 differed little from day 3, averaging 5 μg L-1 in P treatments from 0 to 32 and increasing with successively higher P treatment to 111 μg L-1 in the 256 P treatment.
We aimed to understand the growth and uptake responses of Microcystis to a gradient of phosphorus concentrations during a short, 6-day period after a period of growth in saturating nutrient concentrations. The range of phosphorus concentrations in the experiment were sufficient to reduce phosphorus uptake and growth rates of Microcystis to near zero or below in low phosphorus concentrations and to saturate growth rates in high phosphorus concentrations. Uptake rates were not saturated in high P treatments. We expected growth and uptake physiology of Microcystis to fit Monod, Droop, and Michaelis-Menten model predictions along the phosphorus gradient, but cell growth and phosphorus uptake rates did not fit these models consistently over the 6-day period. Our results are likely due to response of cells to changing phosphorus at the start of the experiment as well as over the course of the 6-day period of the experiment, and they can be explained by the basic physiological theory underpinning the Monod, Droop, and Michaelis-Menten model plus cell phosphorus leakage and intracellular P hoarding in very low P treatments. We will discuss our results and this explanation in the following paragraphs.