Fluctuations in microcystin concentrations, potentially toxic Microcystis and genotype diversity in a cyanobacterial community from a tropical reservoir
Introduction
Cyanobacterial blooms can alter the aquatic food web and can be toxic to wildlife, domestic animals and humans (Codd et al., 2005). Microcystis is the most frequently reported genus in freshwater blooms worldwide (O’Neil et al., 2012, Paerl and Otten, 2013, Srivastava et al., 2013). Some Microcystis strains produce microcystins (MCs), a group of toxic cyclic heptapeptides encompassing more than 80 variants (Dittmann et al., 2013), which are the most common toxins produced by cyanobacterial blooms in freshwater (WHO, 2003, Figueiredo et al., 2004, O’Neil et al., 2012).
In natural populations of cyanobacteria, MC concentrations are determined based on the number of toxin-producing cells and the rate of MC synthesis, which is, in turn, affected by a variety of environmental factors (Figueiredo et al., 2004, Meissner et al., 2013). MC production may be constitutive in cells containing functional mcy genes and may vary 2–3-fold in response to environmental conditions (Meissner et al., 2013, Paerl and Otten, 2013). However, the seasonal variability in MC concentrations during Microcystis blooms exceeds the physiological variability in intracellular MC content reported for isolated Microcystis strains (Kardinaal et al., 2007). Thus, it appears that changes in MC concentrations during the development of Microcystis blooms mainly result from the seasonal succession of toxic and non-toxic genotypes.
The dynamics of Microcystis blooms have recently been studied using molecular techniques, exploring both the diversity and succession of genotypes as well as the variation in the proportion of toxic cells. Studies describing the genotypic diversity of Microcystis populations have reported contradictory findings, showing either selection for specific genotypes during bloom development (Kardinaal et al., 2007, Briand et al., 2009, Kim et al., 2010, Miller et al., 2013) or the maintenance of high genetic diversity within the population (Ye et al., 2009, Pobel et al., 2012, Wang et al., 2012, Zhu et al., 2012). Regarding the detection of mcy+ genotypes during bloom events, in some instances, the proportion of toxic genotypes remained relatively constant and the mcy copy numbers paralleled the Microcystis cell densities, thus prevailing at the peak of the bloom (Yoshida et al., 2007, Ha et al., 2009, Ye et al., 2009, Kim et al., 2010, Te and Gin, 2011, Srivastava et al., 2012). In other cases, the proportion of mcy+ cells varied, and some studies indicated a predominance of toxic genotypes in the emergence and/or senescence phases of a bloom (Kardinaal et al., 2007, Briand et al., 2009, Sabart et al., 2010, Martins et al., 2011). However, several additional cases showed no evidence for a relationship between the proportion of toxic cells and the bloom stage (Hotto et al., 2008, Davis et al., 2009, Conradie and Barnard, 2012, Pobel et al., 2012).
As bloom development is related to environmental factors, many studies have focused on the relationship between the relative abundance of potential MC-producing genotypes and physicochemical variables. Regarding nutrient concentrations, several studies have shown that nitrogen and/or phosphorus levels were positively correlated with the abundance of potentially toxic Microcystis cells (Yoshida et al., 2007, Davis et al., 2009, Davis et al., 2010, Ha et al., 2009, Rinta-Kanto et al., 2009, Te and Gin, 2011, O’Neil et al., 2012, Srivastava et al., 2012). Others indicated that MC-producing genotypes were positively correlated with pH (Ye et al., 2009) or water–surface temperature (Conradie and Barnard, 2012). However, no consensus has emerged to date, as evidenced by the aforementioned studies showing that when a particular abiotic factor is considered, contradictory results are reported, and, in some cases, no strong relationship is observed between any tested physiochemical variable and the abundance of mcy+ cells (Hotto et al., 2008, Martins et al., 2011).
In the majority of frequently cited studies, the correlation between the abundance of toxic genotypes and MC concentrations has been tested. Although positive relationships have been observed in certain cases (Hotto et al., 2008, Davis et al., 2009, Davis et al., 2010, Ha et al., 2009, Rinta-Kanto et al., 2009, Martins et al., 2011, Te and Gin, 2011, Conradie and Barnard, 2012, Srivastava et al., 2012), in other reports, a direct relationship between these two variables is not clear (Ye et al., 2009, Sabart et al., 2010). Furthermore, although cyanobacterial blooms are commonly recorded in the tropics, very few studies have employed molecular tools to investigate the diversity or potential toxicity of these populations compared to temperate and subtropical aquatic environments (Te and Gin, 2011). In temperate aquatic environments, Microcystis experiences a benthic phase during winter followed by recruitment in spring that results in planktonic proliferation and blooms in summer (Brunberg and Blomqvist, 2002, Kim et al., 2010). In contrast, in tropical environments, Microcystis can be found in the water column throughout the entire year, occasionally occurring as the predominant phytoplankton species (Soares et al., 2013). Therefore, an understanding of the dynamics of genotypes and production of MCs in natural populations of cyanobacteria in tropical areas can help reveal factors responsible for the predominance of certain species and prevalence of toxic strains.
In this study, we collected cyanobacterial samples from a eutrophic tropical reservoir where blooms have been recorded annually over the last 15 years (Soares et al., 2009). The three main genera in this system are Microcystis, Cylindrospermopsis and Anabaena, which are also the main bloom-forming genera of cyanobacteria in Brazil (Soares et al., 2013). We tested the hypothesis that MC concentrations can be explained by variations in the number or ratio of toxic genotypes or by the presence of certain genotypes of Microcystis. The results highlight the need to assess whether molecular methods such as qPCR are appropriate for use in MC risk assessment.
Section snippets
Materials and methods
Water samples were collected in the Funil reservoir (22°30′ S, 44°45′ W), Rio de Janeiro, Brazil, from October 2011 to April 2012. This reservoir has an area of 40 km2, a volume of 8.9 × 106 m3, a maximum and medium depth of 70 and 22 m respectively, and a residence time of 41.5 days (Soares et al., 2009). One sample per month was obtained from the integrated euphotic zone (determined as 2.7-times the secchi disk depth) adjacent to the dam. The water temperature and pH were measured using a Yellow
Limnological parameters and phytoplankton dynamics
During the sampling period, the water temperature varied from 24.7 to 29.2 °C, and the chlorophyll-a concentrations ranged from 1.8 to 38.9 μg L−1. High chlorophyll-a levels corresponded to low transparency and high pH (Table 1).
Nutrient concentrations were consistent with a eutrophic environment. DIN values remained high during the entire studied period (maximum of 3044.4 μg L−1, minimum of 477.1 μg L−1). Concentrations of total phosphorus varied from 22.1 to 132.5 μg L−1. However, SRP values remained
Dynamics of cyanobacterial genotype diversity
Studies investigating the diversity of cyanobacterial genotypes in Brazil and other tropical environments, using both isolated strains (Bittencourt-Oliveira et al., 2001, Bittencourt-Oliveira et al., 2011) and natural samples (Dall’agnol et al., 2012, Rigonato et al., 2012, Rigonato et al., 2013), have been scarce, and all previous studies have focused on taxonomic identification. Here, we tracked the transitions in cyanobacterial genotypes throughout a bloom season and we identified 63
Acknowledgments
We are grateful to Lilian Ayres Sá and Eduardo de Freitas Camacho for their technical assistance. This study was conducted under the auspices of the CAPES (Brazil)/NUFFIC (The Netherlands) project 045/2012. This work was supported by the National Council for Scientific and Technological Development – CNPq, INCT-INPeTAm/CNPq/MCT and the Carlos Chagas Filho Foundation for the Support of Science in Rio de Janeiro Development – FAPERJ (E-26/110.747/2012). I.A.G. was supported by a fellowship from
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Environmental factors associated with cyanobacterial assemblages in a mesotrophic subtropical plateau lake: A focus on bloom toxicity
2021, Science of the Total EnvironmentCitation Excerpt :We compared the different driving factors correlated with toxic Microcystis biomass in eutrophic and mesotrophic lakes (Table S5). Temperature and TP, as expected, were the two most mentioned factors triggering the proliferation of toxic Microcystis biomass in the water bodies from eutrophic and hypertrophic lakes (Davis et al., 2009; Guedes et al., 2014; Hu et al., 2016; Joung et al., 2016; Rinta-Kanto et al., 2009; G.L. Yu et al., 2014; L. Yu et al., 2014). Thus, in these lakes, cyanobacterial blooms associated with high MC risks often occur during the summer.