Competition between a toxic and a non-toxic Microcystis strain under constant and pulsed nitrogen and phosphorus supply

Suominen, Saara; Brauer, Verena S.; Ylinen, Anne; Sivonen, Kaarina; Hiltunen, Teppo

doi:10.1007/s10452-016-9603-2

Cited by 25 publications

(17 citation statements)

References 66 publications

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“…In the current study, we observed that the increase in MC-producing phenotypes coincided with a shift in the dissolved inorganic nutrient quota, from phosphorus-limited to nitrogen-limited between the end of August to September ( Supplementary Table S1), suggesting that MC-producing strains are favored over non-MC-producing strains under nitrogen-limiting conditions. This pattern is in line with the experimental results by Suominen et al [71], in which a MC-producing strain performed better than the non-MC-producing mutant under nitrogen limitation. Field studies based on qPCR also indicate that MC-producing strains perform better under low N:P ratios [29,69,72].…”

Section: Discussionsupporting

confidence: 92%

High Diversity of Microcystin Chemotypes within a Summer Bloom of the Cyanobacterium Microcystis botrys

Johansson

Legrand

Björnerås

et al. 2019

Toxins

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The fresh-water cyanobacterium Microcystis is known to form blooms world-wide, and is often responsible for the production of microcystins found in lake water. Microcystins are non-ribosomal peptides with toxic effects, e.g. on vertebrates, but their function remains largely unresolved. Moreover, not all strains produce microcystins, and many different microcystin variants have been described. Here we explored the diversity of microcystin variants within Microcystis botrys, a common bloom-former in Sweden. We isolated a total of 130 strains through the duration of a bloom in eutrophic Lake Vomb, and analyzed their microcystin profiles with tandem mass spectrometry (LC-MS/MS). We found that microcystin producing (28.5%) and non-producing (71.5%) M. botrys strains, co-existed throughout the bloom. However, microcystin producing strains were more prevalent towards the end of the sampling period. Overall, 26 unique M. botrys chemotypes were identified, and while some chemotypes re-occurred, others were found only once. The M. botrys chemotypes showed considerable variation both in terms of number of microcystin variants, as well as in what combinations the variants occurred. To our knowledge, this is the first report on microcystin chemotype variation and dynamics in M. botrys. In addition, our study verifies the co-existence of microcystin and non-microcystin producing strains, and we propose that environmental conditions may be implicated in determining their composition. Key Contribution:This study demonstrates that a single bloom of Microcystis botrys consists of strains with different microcystin chemotypes, each producing from zero up to 12 different microcystin variants. We established that microcystin and non-microcystin producing strains co-occur, and that the chemotype composition varies during the bloom.Toxins 2019, 11, 698 2 of 16 bloom-forming cyanobacteria, and that harmful blooms will increase both in frequency and duration, due to direct and indirect effects of changes in hydrological cycling, increased water temperatures, and nutrient loading [4][5][6][7][8][9].In addition to forming dense blooms which can deteriorate water quality per se, many cyanobacterial genera produce secondary metabolites with significant bioactivity and toxicity to aquatic organisms and humans [10][11][12][13][14]. In freshwaters, microcystins are among the most common cyanotoxins [7,15]. These inhibit the eukaryotic protein phosphatases 1 and 2a, and have hepatotoxic effects in vertebrates [10,16,17]. Drinking water from surface water supplies must therefore be checked for microcystin content, and may not be higher than 1 µg microcystin L −1 according to WHO regulation. Microcystins are cyclic heptapeptides (Figure 1) and are produced by several cyanobacteria including Microcystis, Planktothrix, and Anabaena (Dolichospermum) [14,18,19]. The common structure and biosynthetic pathway of microcystin synthesis in these genera have been described [20][21][22][23][24][25]. In Microcystis, the microcystin synthetase gene cluster co...

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Section: Discussionsupporting

confidence: 92%

High Diversity of Microcystin Chemotypes within a Summer Bloom of the Cyanobacterium Microcystis botrys

Johansson

Legrand

Björnerås

et al. 2019

Toxins

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“…agardhii , but even though the latter reaches a relatively high abundance, the dissolved and particulate content of all three studied MC analogues was found below detection limits. However, the occurrence of non-MC-producing strains of both species is a common phenomenon (Yéprémian et al 2007 ; Park et al 2018 ), and previous studies have indicated that the temporal and spatial distribution of toxic and non-toxic genotypes can be attributed to a number of factors including resource competition (Briand et al 2008 ; Lei et al 2015 ; Suominen et al 2017 ).…”

Section: Resultsmentioning

confidence: 99%

A report of Cylindrospermopsis raciborskii and other cyanobacteria in the water reservoirs of power plants in Ukraine

Rzymski

Horyn

Budzyńska

et al. 2018

Environ Sci Pollut Res

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The occurrence of cyanobacteria in freshwaters attracts much attention due to its associated health threats and ecological implications. Yet data on the composition of cyanobacteria taxa and toxigenicity in some regions is still scarce. Here, we explored the occurrence of cyanobacteria and cyanotoxins in three locations in Ukraine (reservoir for Kasperivtsi Hydrothermal Power Plant and outflowing River Seret, and cooling pond of Khmelnytsky Atomic Power Plant) in summer 2017. Cyanobacteria were a dominant fraction at all stations. A number of potent-toxin producers were identified including Cylindrospermopsis raciborskii, Aphanizomenon gracile, Dolichospermum flos-aquae, and Planktothrix agardhii. Screening for the presence of dissolved and particulate content of microcystins (-LR, -YR, and -RR), cylindrospermopsin, and anatoxin-a yielded negative results. The studied waters displayed no toxicity in human platelets in vitro. Further toxicological and ecological studies are necessary to evaluate the potential presence of cyanotoxin producers in Ukraine.

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“…As reviewed in Suominen et al [191], the differences in microcystin content between genotypes by far outweighs differences induced by resource limitation or temperature. Cooccurrence of genotypes with high and low or no cellular contents of specific metabolites in field populations explains why the microcystin cell quota found in field samples are typically several-fold lower than the maximum cell quota observed in some strains in the laboratory [142,192].…”

Section: Genotype Level Of Peptide Diversity and Dominancementioning

confidence: 99%

“…However, some studies addressing the species level show that not all resource affinity parameters necessarily correlate with cell size and shape [77,199]; niche separation of the morphologically very similar Planktothrix rubescens (red, metalimnetic) and P. agardhii (green, epilimnetic) may serve as an example. Additionally, monoculture experiments with different strains of cyanobacterial species have found distinct differences in their growth traits: Suominen et al [191] report differences in growth characteristics between the Microcystis PPC 7806 wildtype and mcy-knockout mutant, and these differences were sufficiently distinct to model the outcome of competition between both strains with these parameters.…”

Section: Genotype Level Of Peptide Diversity and Dominancementioning

confidence: 99%

“…In a similar experiment with a wildtype of Microcystis and a mcy-knockout mutant, Briand et al [181] found a single pulse of nitrate to strengthen the pre-existing dominance of the non-producing mutant. With the same wildtype and mutant strains, but using semi-continuous cultures instead of batch cultures with nutrient pulses at 3-day intervals, Suominen et al [191] found the opposite response to pulses of nitrate, i.e., dominance of the producing wildtype, but coexistence for up to 30 days in response to pulses of phosphate.…”

Section: Dominance Attained In Competition Experimentsmentioning

confidence: 99%

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Cyanobacteria and Cyanotoxins in a Changing Environment: Concepts, Controversies, Challenges

Chorus

Fastner

Welker³

2021

Water

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Concern is widely being published that the occurrence of toxic cyanobacteria is increasing in consequence of climate change and eutrophication, substantially threatening human health. Here, we review evidence and pertinent publications to explore in which types of waterbodies climate change is likely to exacerbate cyanobacterial blooms; whether controlling blooms and toxin concentrations requires a balanced approach of reducing not only the concentrations of phosphorus (P) but also those of nitrogen (N); how trophic and climatic changes affect health risks caused by toxic cyanobacteria. We propose the following for further discussion: (i) Climate change is likely to promote blooms in some waterbodies—not in those with low concentrations of P or N stringently limiting biomass, and more so in shallow than in stratified waterbodies. Particularly in the latter, it can work both ways—rendering conditions for cyanobacterial proliferation more favourable or less favourable. (ii) While N emissions to the environment need to be reduced for a number of reasons, controlling blooms can definitely be successful by reducing only P, provided concentrations of P can be brought down to levels sufficiently low to stringently limit biomass. Not the N:P ratio, but the absolute concentration of the limiting nutrient determines the maximum possible biomass of phytoplankton and thus of cyanobacteria. The absolute concentrations of N or P show which of the two nutrients is currently limiting biomass. N can be the nutrient of choice to reduce if achieving sufficiently low concentrations has chances of success. (iii) Where trophic and climate change cause longer, stronger and more frequent blooms, they increase risks of exposure, and health risks depend on the amount by which concentrations exceed those of current WHO cyanotoxin guideline values for the respective exposure situation. Where trophic change reduces phytoplankton biomass in the epilimnion, thus increasing transparency, cyanobacterial species composition may shift to those that reside on benthic surfaces or in the metalimnion, changing risks of exposure. We conclude that studying how environmental changes affect the genotype composition of cyanobacterial populations is a relatively new and exciting research field, holding promises for understanding the biological function of the wide range of metabolites found in cyanobacteria, of which only a small fraction is toxic to humans. Overall, management needs case-by-case assessments focusing on the impacts of environmental change on the respective waterbody, rather than generalisations.

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Competition between a toxic and a non-toxic Microcystis strain under constant and pulsed nitrogen and phosphorus supply

Cited by 25 publications

References 66 publications

High Diversity of Microcystin Chemotypes within a Summer Bloom of the Cyanobacterium Microcystis botrys

High Diversity of Microcystin Chemotypes within a Summer Bloom of the Cyanobacterium Microcystis botrys

A report of Cylindrospermopsis raciborskii and other cyanobacteria in the water reservoirs of power plants in Ukraine

Cyanobacteria and Cyanotoxins in a Changing Environment: Concepts, Controversies, Challenges

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