Growth, nitrogen fixation, and nodularin production by two baltic sea cyanobacteria

Abstract

In late summer, nitrogen-fixing cyanobacteria Nodularia spumigena and Aphanizomenon flos-aquae form blooms in the open Baltic Sea. N. spumigena has caused several animal poisonings, but Baltic A. flos-aquae is not known to be toxic. In this laboratory study, performed with batch cultures, the influences of environmental conditions on the biomass and nitrogen fixation rate of N. spumigena and A. flos-aquae were compared and the toxin (nodularin) concentration produced by N. spumigena was measured. Several differences in the biomasses and nitrogen fixation rates of N. spumigena and A. flos-aquae were observed. A. flos-aquae preferred lower irradiances, salinities, and temperatures than N. spumigena. The biomass of both species increased with high phosphate concentrations and with accompanying bacteria and decreased with unnaturally high inorganic nitrogen concentrations. Nodularin concentrations in cells and growth media, as well as nitrogen fixation rates, were generally highest under the conditions that promoted growth. Intracellular nodularin concentrations increased with high temperature, high irradiance, and high phosphate concentration and decreased with low and high salinities and high inorganic nitrogen concentrations. Nodularin concentrations in growth media increased with incubation time, indicating that intracellular nodularin was released when cells lysed. The different responses of A. flos-aquae and N. spumigena to changes in salinity, irradiance, and temperature may explain the different spatial and temporal distribution of these species in the Baltic Sea. According to the results, toxic N. spumigena blooms may be expected in late summer in areas of the Baltic Sea with high phosphorus concentrations and moderate salinity.

Modeling the increase of nodularin content in Baltic Sea Nodularia spumigena during stationary phase in phosphorus-limited batch cultures

“…Our results are consistent with other studies reporting an increase of toxin content at the onset of stationary phase in hepatotoxic cyanobacteria [7,8], and in contradiction with the conclusion that Nod is always a ¢xed proportion of the biomass in N. spumigena [12]. However, in the last study, N. spumigena biomass increase in batch culture was linear rather than exponential, indicating limitation by other factors than claimed phosphorus limitation explaining the di¡erent results.…”

“…We did not detect any Nod in ¢ltered samples in any of our experiments, but it cannot be excluded that small amounts accumulated. In other studies, excretion of Nod was variable, probably depending on the condition of the cells, but the extracellular concentration was usually lower than 50 mg (g Chla) 31 [12], meaning less than 10% of the intracellular concentration. In phosphorus-limited batch culture, the extracellular Nod concentration did not even exceed 4 mg (g Chla) 31 [12].…”

“…The physiology of a phytoplankton cell, and therefore its toxin production, is only directly correlated to concentrations of the limiting nutrient in the medium during steady state growth. The correlation of toxin content in N. spumigena [11,12] and M. aeruginosa [9] with initial nutrient concentration in batch culture can therefore not directly be related to the physiology of toxin production. The more dynamic approach in the current study is a better tool to explain toxin production during non-steady state because the dynamic nature of a batch culture is taken into account.…”

Climate change and regulation of hepatotoxin production in Cyanobacteria

“…In some cases, it appears that increased temperatures may result in decreased toxin production in M. aeruginosa (J€ ahnichen et al, 2011) and in polar cyanobacterial mats incubated at 23°C, (Kleinteich et al, 2012) in contrast to the previously mentioned study (Dziallas & Grossart, 2011). Nodularin production was enhanced at higher temperatures accompanied by higher nitrogen fixation rates (Lehtimaki et al, 1994;Lehtim€ aki et al, 1997). The nontoxic, nitrogen-fixing marine cyanobacterium, Trichodesmium, significantly increased its N 2 and CO 2 fixation rates with increased levels of CO 2 alone (Hutchins et al, 2007) or combined with increased light intensities (Garcia et al, 2011).…”

Meta‐omic analyses of Baltic Sea cyanobacteria: diversity, community structure and salt acclimation

“…Blooms regularly occur during the summer in the central and southern regions of the Baltic Sea (Finni et al, 2001;Stal et al, 2003;Kahru and Elmgren, 2014) and are composed of the diazotrophic (N 2 -fixing) genera Nodularia, Aphanizomenon and Dolichospermum (formerly Anabaena; Wacklin et al, 2009). Besides being important primary producers, providing fixed carbon and nitrogen to higher trophic levels in the ecosystem (Ohlendieck et al, 2000;Stal et al, 2003;Ploug et al, 2010;2011;Motwani and Gorokhova, 2013;Hogfors et al, 2014;Engstr€ om-€ Ost et al, 2015), cyanobacteria produce an array of secondary metabolites, some with documented toxicity (Nehring, 1993;Lehtim€ aki et al, 1997;Landsberg, 2002). The eutrophicationenhanced blooms (Kahru et al, 1994; and their collapse towards the end of the summer season results in a biomass overload that today constitutes an environmental and public health concern.…”