Nitrogen Limitation Promotes Accumulation and Suppresses Release of Cylindrospermopsins in Cells of Aphanizomenon Sp.

Abstract

As the biosynthesis of cylindrospermopsin (CYN) is assumed to depend on nitrogen availability, this study investigated the impact of nitrogen availability on intra- and extracellular CYN and deoxy-CYN (D-CYN) contents in three Aphanizomenon strains from temperate waters. Nitrogen deficient (−N) cultures showed a prolonged growth phase and intracellular toxin accumulation by a factor of 2–6. In contrast, cultures with additional nitrate supply (+N) did not accumulate CYN within the cells. Instead, the maximum conceivable CYN release estimated for dead cells (identified by SYTOX® Green staining) was much lower than the concentrations of dissolved CYN actually observed, suggesting these cultures actively release CYN from intact cells. Furthermore, we found remarkably altered proportions of CYN to D-CYN: as batch cultures grew, the proportion of D-CYN increased by up to 40% in +N medium, whereas D-CYN remained constant or decreased slightly in −N medium. Since +N cultures showed similar toxin patterns as −P cultures with increased extracellular CYNs and higher proportion of D-CYN we conclude that nitrogen limitation may affect the way the cells economize resources, especially the yield from phosphorus pools, and that this has an impact on CYN production and release. For water management, these result imply that nutrient availability not only determines the abundance of potentially CYN-producing cyanobacteria, but also the amount of extracellular CYNs (challenging drinking-water treatment) as well as the ratio of D-CYN to CYN (affecting toxicity).

Constitutive toxin production under various nitrogen and phosphorus regimes of three ecotypes of Cylindrospermopsis raciborskii ((Wołoszyńska) Seenayya et Subba Raju)

“…However, in other freshwater cyanobacterial species capable of CYN production, Q CYN has been shown to differ over the growth cycle and under different light in Oscillatoria (Bormans et al, 2013). It also varies in response to P and N in Aphanizomenon ( Bar-Yosef et al, 2010;Preußel et al, 2009Preußel et al, , 2014, suggesting that CYN may have a different role in these species, or be under different metabolic controls. Ecotype CS-506 had a 6-fold higher Q CYN than CS-505.…”

A Review on the Study of Cyanotoxins in Paleolimnological Research: Current Knowledge and Future Needs

“…As suggested, the lowest CYN levels found in sediments representing the mid-Holocene period correlated with low N/P values, which may be an indication that limited N availability in the lake triggered CYN production [33]. However, experimental data suggests that under N limitation, the release of the toxin is highly suppressed, while additional nitrate supply highly promotes this process [90]. On the other hand, N depletion was demonstrated to cause an increase in intracellular pool [90]-it cannot be ruled out that N-starved cyanobacteria cells deposited in sediments contributed to sedimentary pool of CYN.…”

“…On the other hand, N depletion was demonstrated to cause an increase in intracellular pool [90]-it cannot be ruled out that N-starved cyanobacteria cells deposited in sediments contributed to sedimentary pool of CYN. In contrast, there is experimental evidence that P starvation may induce CYN synthesis and release [76,90,91]. No apparent association of that kind between sedimentary P and CYN levels were found in Lake Griffin.…”

“…However, experimental data suggests that under N limitation, the release of the toxin is highly suppressed, while additional nitrate supply highly promotes this process [90]. On the other hand, N depletion was demonstrated to cause an increase in intracellular pool [90]-it cannot be ruled out that N-starved cyanobacteria cells deposited in sediments contributed to sedimentary pool of CYN. In contrast, there is experimental evidence that P starvation may induce CYN synthesis and release [76,90,91].…”

The surprising world of cyanobacteria: cylindrospermopsin has a soil face

“…Aside from its toxicity aspects, CYN is also interesting from a purely ecological point of view. Several studies have addressed questions regarding conditions that can trigger CYN production/secretion and demonstrated that it is more anticipated under nutrient deficiency (Preußel et al 2014). Could it therefore mediate an adaptive response in an unfavorable environment and physiological stress?…”