Temporal Variations in the Dynamics of Potentially Microcystin-Producing Strains in a Bloom-Forming Planktothrix agardhii (Cyanobacterium) Population

Abstract

The concentration of microcystins (MCs) produced during blooms depends on variations in both the proportion of strains containing the genes involved in MC production and the MC cell quota (the ratio between the MC concentration and the density of cells with the mcyA genotype) for toxic strains. In order to assess the dynamics of MC-producing and non-MC-producing strains and to identify the impact of environmental factors on the relative proportions of these two subpopulations, we performed a 2-year survey of a perennial bloom of Planktothrix agardhii (cyanobacteria). Applying quantitative real-time PCR to the mcyA and phycocyanin genes, we found that the proportion of cells with the mcyA genotype varied considerably over time (ranging from 30 to 80% of the population). The changes in the proportion of cells with the mcyA genotype appeared to be inversely correlated to changes in the density of P. agardhii cells and also, to a lesser extent, to the availability of certain nutrients and the abundance of cladocerans. Among toxic cells, the MC cell quota varied throughout the survey. However, a negative correlation between the MC cell quota and the mcyA cell number during two short periods characterized by marked changes in the cyanobacterial biomass was found. Finally, only 54% of the variation in the MC concentrations measured in the lake can be explained by the dynamics of the density of cells with the MC producer genotype, suggesting that this measurement is not a satisfactory method for use in monitoring programs intended to predict the toxic risk associated with cyanobacterial proliferation.Cyanobacteria in freshwater ecosystems are a source of growing concern, because their proliferation leads to ecological disturbances and the toxins they produce constitute health risks for animals as well as human beings (4, 24). These microorganisms are known to produce numerous bioactive secondary metabolites (reviewed in reference 62), which can be toxic (64). These metabolites include microcystins (MCs), which are the most commonly occurring cyanotoxins and have been involved in several poisonings of animals and human beings (7). MCs are hepatotoxic cyclic heptapeptides (for their general structure and nomenclature, see reference 6) synthesized nonribosomally by a multifunctional enzyme complex (13). The gene cluster coding for this enzyme complex consists of 9 or 10 genes, depending on the genus. The corresponding genes of Microcystis aeruginosa 53), Planktothrix agardhii CYA 126 (9), and Anabaena sp. strain 90 (44) have been completely sequenced.The concentration of MCs in cells or in the water during a cyanobacterial bloom cannot be predicted. This is partly because of differences in the proportions of MC-producing and non-MC-producing subpopulations within cyanobacterial populations (27, 58, 59) and partly because of toxin heterogeneity within an MC-producing subpopulation (65) and/or differences at the level of the expression of the genes involved in the biosynthesis of these molecules (16,20). One of the most inte...

Cyanobacterial dynamics and toxins concentrations in Lake Alto Flumendosa, Sardinia, Italy

“…The 'average' density-based P. rubescens cell quota determined in this study were in the range of other values reported in literature (Naselli-Flores et al, 2007;Briand et al, 2008;Kosol et al, 2009;Manganelli et al, 2010Manganelli et al, , 2016. Interestingly, the cell quota determined for M. botrys were constantly about 10 times higher than P. rubescens and in the range of Microcystis cell quota in the field estimated by Yu et al (2014) (0.001 and 1.326 pg cell -1 on the whole population and 0.012 and 1.876 pg cell -1 on the toxic cells).…”

“…The quantification of mcy genes of P. rubescens has been indicated as a better predictor of MC concentrations (Ostermaier and Kurmayer, 2010;Hautala et al, 2013). However, in this study the application of the linear regression to the mcyB + cells and MC reduced the percentage of MC variation explained, from >80% to ~50%, i.e., a value very close to what was observed by Briand et al (2008) in a population of P. agardhii and consistent with what we previously described in Lake Vico (Manganelli et al, 2016). There are several possible explanations for this outcome, as summarized in Kurmayer et al (2016), such as other coexisting non identified toxic species, problems in the amplification of mcy genes or mutation inactivating mcy genes.…”

Bacterial degradation of dissolved organic matter released by Planktothrix agardhii (Cyanobacteria)

“…There are many studies about cyanotoxins degradation, including microcystins produced by P. agardhii (Chen et al, 2008;Kormas and Lymperopoulou, 2013). However, besides its importance as a biomass producer and potentially toxic products (Briand et al, 2008;Tonk et al, 2005), almost no data can be found on the destination of DOC and how this process may affect the establishment and maintenance of the local bacterial community.…”

Genetic analysis on Dolichospermum (Cyanobacteria; sensu Anabaena) populations based on the culture-independent clone libraries revealed the dominant genotypes existing in Lake Taihu, China

“…Cyanobacterial blooms not only produce different kinds of toxins (microcystins, anatoxin-a, cylindrospermopsin, etc. ), but also synthesize and release odor compounds (2-methylisoborneol (2-MIB), Geosmin) (Briand et al, 2008;Graham et al, 2010;Wang et al, 2011). Among the water bloom forming cyanobacterial genera, Microcystis, Planktothrix, Dolichospermum (formerly as planktonic species in Anabaena genus) (Wacklin et al, 2009), and Aphanizomenon are usually the rulers governing the freshwaters and producing numerous bioactive secondary metabolites over the world (Pan et al, 2009;Vaitomaa et al, 2003).…”