Relationship between Photosynthetic Capacity and Microcystin Production in Toxic Microcystis Aeruginosa under Different Iron Regimes

Abstract

Blooms of harmful cyanobacteria have been observed in various water bodies across the world and some of them can produce intracellular toxins, such as microcystins (MCs), which negatively impact aquatic organisms and human health. Iron participates significantly in cyanobacterial photosynthesis and is proposed to be linked to MC production. Here, the cyanobacteria Microcystis aeruginosa was cultivated under different iron regimes to investigate the relationship between photosynthetic capacity and MC production. The results showed that iron addition increased cell density, cellular protein concentration and the Chl-a (chlorophyll-a) content. Similarly, it can also up⁻regulate photosynthetic capacity and promote MC⁻leucine⁻arginine (MC⁻LR) production, but not in a dose⁻dependent manner. Moreover, a significant positive correlation between photosynthetic capacity and MC production was observed, and electron transport parameters were the most important parameters contributing to the variation of intracellular MC⁻LR concentration revealed by Generalized Additive Model analysis. As the electron transport chain was affected by iron variation, adenosine triphosphate production was inhibited, leading to the alteration of MC synthetase gene expression. Therefore, it is demonstrated that MC production greatly relies on redox status and energy metabolism of photosynthesis in M. aeruginosa. In consequence, more attention should be paid to the involvement of photosynthesis in the regulation of MC production by iron variation in the future.

Keywords: Microcystis aeruginosa; cyanobacterial growth; iron; microcystin production; photosynthetic capacity.

Figure 1

Cell density (a), protein content (b) and Chl-a (chlorophyll-a) content (c) of M. aeruginosa (Microcystis aeruginosa) FACHB–905 under different iron conditions. Error bars represent the standard deviation of triplicate samples. a, significant difference between 10 μM exposure and control exposure on the same cultivation day; b, 20 μM–0 μM; c, 40 μM–0 μM; d, 60 μM–0 μM; e, 80 μM–0 μM; f, 100 μM–0 μM. p < 0.05 was accepted as statistically significant for differences.

Figure 2

Photosynthetic parameters of M. aeruginosa (Microcystis aeruginosa) exposed to different iron concentrations ((a): F_v/F_m, maximal quantum yield, dimensionless; (b): rETR_max, maximal relative electron transport rate, μmol electrons m⁻² s⁻¹; (c): α, photosynthetic efficiency, μmol electrons m⁻² s⁻¹/μmol photos m⁻² s⁻¹). Error bars represent the standard deviation of triplicate samples. a Significant difference between the sampling day and the 2nd day under the same iron exposure; * Significant difference between the iron addition exposure and the control exposure on the same cultivation day. p < 0.05 was accepted as statistically significant for differences between exposure data.

Figure 3

Intracellular (a) and extracellular (b) MC–LR concentration of M. aeruginosa (Microcystis aeruginosa) FACHB–905 under different iron conditions. Error bars represent the standard deviation of triplicate samples.

Figure 4

Relationship between physiological activity and intracellular MC–LR concentration of M. aeruginosa FACHB–905 ((a): Chl-a (chlorophyll-a) content, n = 70; (b): F_v/F_m, maximal quantum yield, n = 35; (c): rETR_max, maximal relative electron transport rate, n = 35; (d): α, photosynthetic efficiency, n = 35). Both the R² and significance level are indicated; *** p < 0.001.

Figure 5

Chl-a (chlorophyll-a) (a), F_v/F_m (b), rETR_max (c) and α (d) effect curves from a GAM model fitted to intracellular MC–LR concentration data (solid lines), with two 95% confidence bands (dashed lines). R², significance level and explained deviation are indicated; *** p < 0.001.